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For vision, insect and vertebrate eyes use rhabdomeric and ciliary photoreceptor cells, respectively. These cells show distinct architecture and transduce the light signal by different phototransductory cascades. In the marine ragworm Platynereis, we find both cell types: rhabdomeric photoreceptor cells in the eyes and ciliary photoreceptor cells in the brain. The latter use a photopigment closely related to vertebrate rod and cone opsins. Comparative analysis indicates that both types of photoreceptors, with distinct opsins, coexisted in Urbilateria, the last common ancestor of insects and vertebrates, and sheds new light on vertebrate eye evolution.
In animal photoreceptor cells (PRCs), the surface membrane is enlarged for the storage of opsin photopigment (1). Two major types of PRCs are recognized by electron microscopy (table S1). In rhabdomeric PRCs, the apical cell surface folds into microvilli. This is the predominant type of PRC used for vision in invertebrates. In contrast, in vertebrates, the rods and cones of the retina and the PRCs of the pineal eye, a light-sensitive structure in the dorsal diencephalon, are of the ciliary type. In ciliary PRCs, the membrane of the cilium is folded for surface enlargement. To elucidate the evolution of ciliary PRCs, we investigated the photosensitive system in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa) (2, 3). This species shows ancestral anatomy and development and an ancestral gene inventory (2, 4). In addition, polychaetes and vertebrates are evolutionarily far apart (2), and thus any feature specifically shared between them as a result of their common evolutionary heritage necessarily existed in Urbilateria, the last common ancestor of all animals with bilateral symmetry.
Platynereis develops different pairs of eyes (5), as demarcated by opsin expression in Fig. 1A: "larval eyes," implicated in larval phototaxis, and "adult eyes," active in adult vision. All these eyes use rhabdomeric PRCs. The two pairs of adult eyes originate from a single anlage that is not yet split at the stage of the analysis. To identify ciliary PRCs, we used an antibody directed against acetylated α-tubulin (Fig. 1A) (3), which specifically labels stabilized microtubules in cilia and axons. In addition to the axonal scaffold, we detected two paired structures in the developing median brain, on the dorsal side of the apical organ (Fig. 1A, arrows). Electron microscopy (3) revealed that these...