Looking back on why we look forward: A special research series by Adam Glover, Part 2

The incredible diversity in eye morphology within the animal kingdom led previous researchers to believe these different forms evolved independently of one another. However, studies of embryological development, genetics, and morphology across lineages suggest that the wide variety of eyes we see in the animal kingdom today- including the complex camera eye of modern humans- may have evolved from the same ancestral light sensitive organ (Fernald, 2000).  Support for the idea of a single ancestral light sensitive organ stems from the finding that the photoreceptors, phototransduction pathways, and genetic controls of eye development are homologous in all visual systems. The development of all visual organs is mediated by the same gene, called the PAX6 gene (PAX6 codes for proteins that bind to DNA in such a way that the genes involved in the formation and regulation of eye structures are turned on) (Quiring et al., 1994); all photoreceptors, both rhabdomeric and ciliary (those utilized in invertebrate compound style eyes and vertebrate camera style eyes, respectively), use a light sensitive pigment derived from vitamin A which is bound to a protein called opsin (Eakin, 1979); and a common phototransduction pathway is found in all visual organs such that when light strikes these photopigments, a conformational change is induced in the photopigment which activates opsin and opsin then binds to a G-protein used in a signal transduction cascade (Ranganathan etal., 1995).

It is thought that prior to acquiring the elements necessary to operate as a visual organ “eyes” functioned to detect light for modulating circadian and seasonal rhythms. Evidence for this stems from the areas of comparative anatomy and developmental biology; because aspects of an organism’s embryological development are known to reflect events that occurred during the evolution of its lineage, and because it has been found that during development the eyes of both jawless and jawed vertebrates (both of which have a complex camera style eye with ciliary photoreceptors) pass through a stage in which they resemble those of the nonvisual hagfish (which use their “eyes” to modulate such rhythms), it has been hypothesized that an ancestral light sensing organ would take a hagfish-like form and modulate circadian and seasonal rhythms (Lamb, 2011).

Intermediate structures which show states between an ancestral patch of light sensitive cells and our modern eye are obviously many; one of the most radical shifts of this evolutionary process occurred when the ancestral precursor photoreceptor cell that used an ancestral opsin for light detection involved in seasonal/circadian rhythms duplicated its opsin gene into two paralogs, c-opsin and r-opsin, allowing the diversification of the precursor photoreceptor cell into ciliary and rhabdomeric sister cell types (Arendt etal., 2004).  As previously mentioned, rhabdomeric and ciliary photoreceptor cells are utilized in invertebrate compound style eyes and vertebrate camera style eyes, respectively.The two cell types differ in their strategy for increasing membrane surface area, which allows for increased incorporation of opsins since its complex with a photoreceptor molecule needs to be imbedded in a membrane. Rhabdomeric photoreceptors increase their surface area by densely folding their apical surfaces, while ciliary photoreceptors increase their surface area by modifying the cilium such that the ciliary membrane folds and stacks on top of itself like a stack of discs. As this relates to intermediate eye structures within our lineage, one recent and novel finding suggests that the output neurons of the vertebrate camera style eye (which send information from the retina to the brain) are actually the descendants of rhabdomeric photoreceptors (Arendt, 2003). This could explain how the evolutionary line which led to vertebrates incorporated both photoreceptor types into its retina yet eventually spawned the strictly ciliary eyes of modern humans.

Continued findings of intermediate structures like this further supports the idea that Homosapiens complex camera style eye evolved from the same toolkit of photoreceptors that invertebrates utilized to develop a compound eye (Fernald, 2000). Homosapiens and other primates, however, differ from other mammals that share this common ancestor in deep time- they specialize in vision as their primary sense (Allman, 1977). This specialization is expressed in part by their characteristic anteriorly directed convergent eye orbits. What selection pressures favored anteriorly directed  convergent eye orbits in ancestral primates? The hypotheses are many, and the purpose of this paper is to review the scientific literature relevant to this question such that a conclusion can be made and its broader implications can be explored.