Eye evolution and the origin of Darwin's eye prototype

In The Origin of Species, Darwin proposed that the complex eyes of animals evolved from a simple prototype consisting of two cells only, a photoreceptor cell and a pigment cell shielding the light from one side and allowing for a directional vision. The discovery of Pax6 as a master control gene for eye development in bilateria lends considerable support to the hypothesis of a monophyletic origin of the metazoan eyes from a Darwinian prototype. Pax6 is found in all bilateria and it is capable of inducing ectopic eyes in both vertebrates and invertebrates. The Darwinian prototype eyes have been found in nature in certain planarians and in the trochophora larvae of Platynereis, an annelid worm, where they were found to express Pax6. The prototypic eye must have evolved from a single cell. Such a single-celled pigmented photoreceptor has been found in the larvae of Tripedalia, a jellyfish, whereas the adult has multicellular lens eyes. We propose that the evolution of the prototypic eye started with a first step of cellular differentiation from a single-celled pigmented photoreceptor, into two cell types: a photoreceptor cell specified by Pax6, and a pigment cell specified by the microphthalmia transcription factor (Mitf), which is also conserved from jellyfish to humans. From the prototypic eye more complex eyes can evolve by intercalating additional genes into the eye developmental pathway by gene duplication and subsequent divergence or by enhancer fusion.