Eye story

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In this part of the lecture, we continued to explore the evolution of the visual system, this time in metazoans. First, we introduced rhabdomeric and ciliary receptors and used this distinction to shed light on an evolutionary point concerning our own ganglion cells (RGCs). We followed Detlev Arendt and colleagues and showed that both types of receptor are found in polychaetes, and that these receptors did not really disappear in vertebrates, but gave rise to retinal ganglion cells.

Going further back in evolution, we find that Ciona intestinalis, the closest protochordate to vertebrates , has a light-sensitive organ (ocelli) containing a few ciliary photoreceptors and a large pigment cell (practically Darwin's prototype). Light in the Cione is hyperpolarizing (as in vertebrates) and there is only one opsin.

This has led to the following evolutionary scenario: a primitive chordate with a pair of amphioxus- or Cione-type photoreceptor organs (which probably lost 1), expanded laterally and developed into a 2-layer retina, with ciliary photoreceptors contacting projection neurons (probably rhabdomeric receptors) giving a mixine-type eye generating circadian behavior and shadow recognition capability. This was followed by the acquisition of a lens (lamprey) and an increase in computational capacity through the introduction of bipolar cells between photoreceptors and RGCs. The RGCs would then be projected to the thalamus (and not just the hypothalamus).

We then returned to the controversy over whether vision is monophyletic or polyphyletic. The three main examples are vertebrates, arthropods and molluscs (cephalopods). It has long been thought that the origins of the eyes in these three phyla were different, due to the different origins of the tissues that make up the eye, mentioned above.

In cephalopods, invagination of the ectoderm is at the origin of the eye, whereas in vertebrates, a cerebral component is decisive (retina and pigment epithelium), inducing the lens (ectoderm). In arthropods, we have compound (faceted) eyes of ectodermal origin, as in cephalopods, but with a very different organization. In clams and scallops (bivalves), the eyes are not cephalic in origin.

For some, these differences suggest distinct origins and argue in favor of convergent evolution. The eyes would have evolved independently and several times, for some authors from 40 to 65 times. This is quite unthinkable. Gehring makes the strongest case for a monophyletic origin. From the eyeless (fly), small eye (mouse) and aniridia (human) mutations, the "same" Pax6 gene was cloned. This conservation strongly suggests that Pax6 played a role in the development of the Bilateria eye since, if arthropods and vertebrates need it to build the eye, their common ancestor probably did too.

We can therefore follow Gehring when he proposes that all Bilateria eyes can be traced back to the Darwinian prototype similar to that of planarians, but that the rest is based on divergent, convergent or parallel evolutionary processes. Gehring proposes two evolutionary hypotheses. In the first, metazoans were formed by the assembly of a colony of flagellated cells, with subsequent specialization into pigmentary and receptor cells.

In a second scheme, Gehring takes up the symbiont hypothesis, based on Chlamydomonas, with the intuition that light perception can be traced back to cyanobacteria that integrated into eukaryotes in the form of chloroplasts. As we have seen, Gehring proposes that dinoflagellates transferred their photoreception genes to the cnidarians of which they are symbionts.

Studies on Pax6 expression during development are limited to arthropods and vertebrates. The origin of the Pax genes predates that of the eyes and nervous system, since they are found in sponges and eyes only appear with cnidarians. But even in cnidarians, there are no direct homologs of Pax6.

However, Pax B, which most probably gave rise to Pax4/6 and Pax2/5/8 by duplication, is expressed in the eyes of hydrozoans (Cladonema) and cubozoans (Tripedalia), which are cnidarians. We can hypothesize that PaxB in these species plays the role of Pax6 in eye development, but that the direct involvement of Pax6 or the Pax-Six-Eya-Dach genetic "consortium" post-dates the divergence of cnidarians from bilaterally symmetrical organisms.

In conclusion, we can't forget that organisms without eyes (such as cnidarians or, closer to home, nematodes) also express Pax genes. But this cannot be taken as an argument against a monophyletic origin. In fact, it's even probable that the invention of the eye or vision was based on a refinement of chemoreception.