Extensive opsin gene expansion and non-cerebral origin of the minimalist eye in a model tardigrade
Panarthropod vision exhibits extraordinary morphological and functional diversity, yet the sensory biology of tardigrades--microscopic extremophiles renowned for their resilience--remains poorly understood. In the model tardigrade Hypsibius exemplaris, we uncover an unprecedented expansion of opsin genes, with over 100 paralogs constituting the largest known opsin repertoire in any animal. Paradoxically, the visual system is structurally minimalist: a paired, inverse pigment-cup ocellus embedded within the brain lobes, forming a single-pixel, dual-receptor organ. Integrating genomic, phylogenetic, molecular expression, and ultrastructural analyses, we show that directional vision relies on a single rhabdomeric opsin (He-R-Opsin-V), localized to microvilli of the rhabdomeric cell. A ciliary photoreceptor with a lamellated cilium co-expresses two ciliary opsins (He-C-Opsin-1 and -2), suggesting non-visual light detection. These and other non-visual opsins are differentially expressed in the brain, gut, storage cells, and peripheral tissues, implicating them in circadian regulation, neuromodulation, ecdysis, digestion, and environmental sensing. Crucially, the eye is an internalized epidermal vesicle, not a cerebral derivative, challenging long-standing assumptions about its evolutionary origin. These findings reveal how extreme miniaturization drives sensory system simplification in visual organs while enabling parallel evolutionary innovation in non-visual photoreception. This study establishes a new paradigm for sensory evolution in microscale animals.