Evolution of the vertebrate retina by repurposing of a composite ancestral median eye
George Kafetzis, Michael J. Bok, Tom Baden, Dan-Eric Nilsson
Abstract
The vertebrate retina is a uniquely complex and evolutionarily conserved structure, combining ciliary (rod and cone) and rhabdomeric (ganglion, amacrine and horizontal cells) photoreceptor lineages within a multilayered circuit. This arrangement contrasts with the ancestral bilaterian cephalic pattern, where rhabdomeric photoreceptors dominate lateral eyes and ciliary photoreceptors are largely limited to unpigmented, non-visual median positions. Here, we make a case that the vertebrate retina evolved through the lateralization of a complex median photoreceptive organ already containing both photoreceptor types. This shift likely followed the loss of lateral rhabdomeric eyes in a burrowing, suspension-feeding deuterostome ancestor that retained a pool of median photoreceptors. In the early chordates leading to vertebrates, this structure diversified into the pineal/parapineal complex and lateral retinas. Central to this transformation was the emergence of a bipolar cellular identity, linking ciliary and rhabdomeric circuits - an unusual feature in animal nervous systems. We suggest that bipolar cells predate the retina and have dual evolutionary origins: Off bipolar cells deriving from a ciliary 'effector' lineage and rod-On bipolar cells deriving from a chimeric sensory cell. This model explains key similarities between the retina and the pineal gland and supports a scenario in which vertebrate vision emerged by integrating and repurposing preexisting circuits. It reframes the retina not as a de novo innovation, but as a modified and lateralized solution to sensory challenges faced by early chordates.