Prolific Origination of Eyes in Cnidaria With Co-Option of Non-Visual Opsins

Abstract

Animal eyes vary considerably in morphology and complexity, and are thus essential for understanding the evolution of complex biological traits. While eyes evolved many times in bilaterian animals with elaborate nervous systems, image-forming and simpler eyes also exist in cnidarians, ancient non-bilaterians with only simple neural nets to process information. How often eyes of varying complexity, including image-forming eyes, arose in animals with such simple neural circuitry remains obscure. Here, we produced large-scale phylogenies of Cnidaria and their photosensitive proteins and coupled them with an extensive literature search on eyes and light-sensing behavior to show that cnidarian eyes originated at least eight times, with complex, lensed-eyes having a history separate from other eye types. Compiled data show widespread light-sensing behavior in eyeless cnidarians and comparative analyses support ancestors without eyes that already sensed light with dispersed photoreceptor cells. The history of expression of the photoreceptive protein opsin supports the inference of distinct eye origins via separate co-options of different non-visual opsin paralogs into eyes. Overall, our results show that eyes evolved repeatedly from ancestral photoreceptor cells in non-bilaterian animals with simple nervous systems, co-opting existing precursors, similar to what occurred in Bilateria. Our study underscores the potential for multiple, evolutionarily-distinct visual systems and underlying developmental pathways, even in animals with simple nervous systems.