A median eye origin of the vertebrate retina explains its unique circuitry

Abstract

The vertebrate retina is a uniquely complex and evolutionarily conserved structure among bilaterians, combining ciliary (rods and cones) and rhabdomeric (ganglion, amacrine, and horizontal) 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 limited to unpigmented, non-visual median positions. We propose 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 and the retention of a median eye. 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 bipolar cells have dual evolutionary origins: Off bipolar cells from a ciliary effector lineage and rod- On bipolar cells from a chimeric sensory cell. This model explains key similarities between retina and pineal 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.