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an ancient origin for the human eye

We understand a fair bit, these days, about the evolution of the complex, 'camera-type' vertebrate eye. Not that this has stopped creationsists (most recently the 'intelligent design' camp as represented by the Discovery Institute) from arguing that the eye is an excellent example of How Evolution Is Wrong - what, they ask, is the use of half an eye? (The answer is, plenty, if an organism can detect the direction of a light source, or the movement of a predator - & in fact it's been suggested that the evolution of even the most basic photoreceptors may have had a hand in the rapid increase of animal taxa during the Cambrian.)

However, one of the unanswered questions (& thus fertile ground for creationists) has always been, when? Just how deep in time is the origin of the vertebrate eye & its specialised light receptors. A new paper just out may help us to answer that question (Passamaneck et al. 2011).

Passamaneck and his co-workers examined photoreception in larval brachiopods. As a child, I first knew this group of animals by the name 'lamp shells', because one of the two shelly valves that encloses the animal's body looks a bit like an ancient Roman oil lamp. I've still got a couple of shells somewhere around - & also a fossil brachiopod endocast, fetchingly called a 'vulva stone' because of its apparent resemblance to a portion of the female human anatomy.

Brachiopods are a taxon of marine invertebrates with a reasonably long fossil history - their remains have been found in rocks dating back to the early Cambrian, more than 500 million years ago. Along with the majority of other animal phyla brachiopods are 'protostomes': a grouping based on a number of shared embryonic features but named for the fact that when the embryonic gut is forming, the opening that will become the mouth develops first, ahead of the anus. Chordates like us, on the other hand, are 'deuterostomes' and yes, you've guessed it, the mouth forms after the anus :-)

So, you might expect organisms so different as mammals & brachiopods, seperated by such a gulf of evolutionary time, to have different means of detecting light. According to Passamaneck & his colleagues, you'd be wrong.

Both chordates such as ourselves and the invertebrates (including brachiopods) are bilaterally symmetrical. Passamaneck et al. argue that there is good evidence for "the coexistence of both [ciliary and rhabdomeric] photoreceptor types in the last common bilaterian ancestor" of chordates and invertebrates. (That post of PZ's that I've just linked to gives a really good description of the two types of light detectors in bilaterally symmetrical animals, and the paper I'm talking about takes that work another step forward.) However, scientists have generally thought that only vertebrates' "cerebral eyes" (ie eyes intimately linked to the brain) use ciliary photoreceptors to detect the direction of light sources, while invertebrates use rhabdomeric receptors for this task. Passamaneck's team decided to test the hypothesis that protostome invertebrates' cerebral eyes use only rhabdomeric photoreceptors, using larvae of the brachiopod Terebratalia transversa as a test case. To do this they collected data on the structure & morphology of these eyes, and also on patterns of expression of the relevant genes.

Protostomes do have ciliary photoreceptors, by the way, but up until now it's appeared that they're usually found deep in the 'brain' of protostomes & have non-visual functions ie they're not involved in detecting light stimuli. However, because the pigments are similar to those expressed in the rods & cones of our eyes, there's the suggestion of common ancestry. It's been hypothesised that over time these receptors migrated to the surface of the body & acquired visual functions on the way.

Fully developed, swimming T.transversa larvae have two rows of pigmented spots, described as eye spots, at the anterior end of their bodies. (Younger, non-swimming larvae don't have them.) The research team determined that these spots are effectively simple eyes made up of 2 photoreceptor cells. One of these cells has a lens-like structure & the other, pigment granules, and both have extensive ciliary membranes positioned between lens & pigment. In addition, each cell of each eyespot is linked by a nerve cell to the larval 'brain', which justifies their description as cerebral 'eyes'. (The 'brain' of these larvae is perhaps better described as a cerebral ganglion: a concentration of nerve cells at the anterior end of the animal's body.) In other words, the researchers found that this protostome species had ciliary photoreceptors on the body surface, rather than the expected rhabdomeric receptors. And this in turn suggests that a key feature of the vertebrate eye, the ciliary receptors that we know as rods & cones, goes back a very long time indeed, to the last common ancestor of protostomes and deuterostomes.

The team went on to look at the expression of a particular gene related to light reception - a c-opsin - cloned from T.transversa. They concluded that this gene was similar to opsins found in other bilaterally symmetrical animals (whether proto- or deuterostome), and that this similarity was due to the groups having shared a common ancestor that also possessed this opsin molecule. And in Terebratalia larvae this c-opsin is expressed in the eyespots, which also supports the idea that they use ciliary photoreceptors. Also, these photoreceptors are definitely used in detecting and responding to directional stimuli: placed in a phototaxis chamber with a light source to one side, swimming larvae moved towards the light source, but went back to a fairly even distribution in the chamber when the light was switched off.

All this led the team to decide that

While ciliary photoreceptors are not the predominant form in the larval cerebral eyes of protosomes, they are found in a phylogenetically diverse range of taxa. It should, therefore, be considered that the use of ciliary photoreceptors in eyes may [possibly] be an ancestral condition for... Bilateria.

In other words, the complex mammalian eye has is evolutionary roots in something akin to the simple eyespots of a tiny marine invertebrate larva.

I wonder what the Discovery Institute will make of that?

Passamaneck YJ, Furchheim N, Hejnol A, Martindale MQ, & Luter C (2011). Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo, 2 (1) PMID: 21362157

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We already knew that both the c-opsin and the r-opsin family (each with its separate chemical cascade for amplifying the energy of a photon) go back in evolution before early bilaterian animals diverged into protostomes and deuterostomes. The theory has it that in chordate eyes, the cells that were originally rhabdomeric photoreceptors were repurposed as ganglion cells in the retina. In the human eye, some of those cells still express melanopsin -- which belongs to the r-opsin family -- but they seem to be involved in the pupil responses, rather than for forming images.

Conversely, in protostomes such as the polychaete worm that PZ writes about in the Pharyngula post you mentioned, it's the other way around: the image-forming eyes use r-opsin photoreceptors while the c-opsin cells serve broader light-response purposes.

I think some molluscs use both kinds for image-forming eyes, but can't be bothered looking up the details. Anyway, your point is that it just got more complex.

In fact the history of vision goes back further than that, back before bilateria separated from cnidaria, because jellyfish have photoreceptors too (and image-forming eyes in the case of box jellies), of the ciliary kind, with pigments from the c-opsin family.

But wait, there's more! There's a third broad family of photopigments, the G[0]-coupled opsins, which turn up (sporadically) across the bilateria... and jellyfish have them too!

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