Keep an Eye on the Argonauta! A Comparative Evolutionary Analysis of Key Genes for Vision in Littoral Versus Deep-Sea Octopuses

The ability to detect light and process visual information is crucial to octopods’ success, allowing environment exploration, food detection, predator avoidance, and exceptional camouflaging. These is made possible by their complex camera-like eyes and highly developed optic lobes. However, data on octopod photoreception, particularly in deep-sea species, remain scarce. To address this gap, adaptations to various light conditions among different octopod species living in diverse environments were investigated by examining differences in their molecular light-sensing machinery, the opsins.<br><br> To begin, the ancestral opsin toolkit of octopods was reconstructed, revealing that their common ancestor possessed at least five opsins: r-opsin1, r-opsin2, xenopsin, retinochrome, and peropsin. Additionally, a novel group of opsin-like molecules, termed pseudopsins, was identified. These molecules lack the retinal-binding domain, which is essential for photoreception.<br><br> Furthermore, RT-qPCR analysis was conducted to examine the expression patterns of these various opsins in two distantly related octopods, <i>Argonauta argo</i> and <i>Octopus vulgaris</i>, revealing a complex expression pattern: r-opsin1 is expressed in the retina, optic lobe, and suckers; r-opsin2 in the optic lobe; xenopsin in the retina; retinochrome in all tissues; peropsin in the optic lobe; and pseudopsin in all tissues. These findings raise new questions about the role of opsins in non-photoreceptive tissues and the function of xenopsin, which is capable of activating a signalling cascade in cephalopod eyes.<br><br> Next, low-coverage RNA sequencing of the visual system (retina and optic lobe) was performed on five octopod species inhabiting different light environments. These data were used to perform a positive selection analysis on the two most highly expressed opsins in the eye, r-opsin1 and retinochrome. Among the species studied, positive selection was observed in r-opsin1 only in <i>Pteroctopus tetracirrhus</i> living in the bathypelagic environment. In contrast, retinochrome exhibited positive selection sites in all deep-sea species, providing new insights into the evolution of these molecules.