Molecular Evolution of Spider Vision: New Opportunities, Familiar Players.

Spiders are among the world's most species-rich animal lineages, and their visual systems are likewise highly diverse. These modular visual systems, composed of four pairs of image-forming "camera" eyes, have taken on a huge variety of forms, exhibiting variation in eye size, eye placement, image resolution, and field of view, as well as sensitivity to color, polarization, light levels, and motion cues. However, despite this conspicuous diversity, our understanding of the genetic underpinnings of these visual systems remains shallow. Here, we review the current literature, analyze publicly available transcriptomic data, and discuss hypotheses about the origins and development of spider eyes. Our efforts highlight that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages. For example, many (but not all) of the genes that appear important for early eye development in spiders are familiar players known from the developmental networks of other model systems (e.g., Drosophila). Similarly, our analyses of opsins and related phototransduction genes suggest that spider photoreceptors employ many of the same genes and molecular mechanisms known from other arthropods, with a hypothesized ancestral spider set of four visual and four nonvisual opsins. This deep homology provides a number of useful footholds into new work on spider vision and the molecular basis of its extant variety. We therefore discuss what some of these first steps might be in the hopes of convincing others to join us in studying the vision of these fascinating creatures.

Opsin Expression in the Central Nervous System of the Mantis Shrimp Neogonodactylus oerstedii.

Visual pigments, each composed of an opsin protein covalently bound to a chromophore molecule, confer light sensitivity for vision. The eyes of some species of stomatopod crustaceans, or mantis shrimp, can express dozens of different opsin genes. The opsin diversity, along with spectral filters and unique tripartite eye structure, bestow upon stomatopods unusually complex visual systems. Although opsins are found in tissues outside typical image-forming eyes in other animals, extraocular opsin expression in stomatopods, animals well known for their diversity of opsins, was unknown. Caudal photoreception in the central nervous system of decapod crustaceans, a group closely related to stomatopod crustaceans, is thought to be opsin based. However, electrophysiological data suggest that stomatopods do not have caudal photoreceptors. In this study, we identified mRNAs that could encode four different opsins and several components of a potential Gq-mediated phototransduction pathway in the central nervous system of the Caribbean mantis shrimp Neogonodactylus oerstedii. The four opsins are abundantly expressed in the cerebral ganglion, or brain, with little or no expression in the remainder of the ventral nerve cord. Our data suggest that there are previously undiscovered cerebral photoreceptors in stomatopods.

Opsins and Their Expression Patterns in the Xiphosuran Limulus polyphemus.

The American horseshoe crab Limulus polyphemus (Linnaeus, 1758) is one of four extant species of xiphosuran chelicerates, the sister group to arachnids. Because of their position in the arthropod family tree and because they exhibit many plesiomorphic characteristics, Xiphosura are considered a proxy for the euchelicerate ancestor and therefore important for understanding the evolution and diversification of chelicerates and arthropods. Limulus polyphemus is the most extensively studied xiphosuran, and its visual system has long been a focus of studies critical for our understanding of basic mechanisms of vision and the evolution of visual systems in arthropods. Building upon a wealth of information about the anatomy and physiology of its visual system, advances in genetic approaches have greatly expanded possibilities for understanding its biochemistry. This review focuses on studies of opsin expression in L. polyphemus, which have been significantly advanced by the availability of transcriptomes and a recent high-quality assembly of its genome. These studies show that the repertoire of expressed opsins in L. polyphemus is far larger than anticipated, that the regulation of their expression in rhabdoms is far more complex than anticipated, and that photosensitivity may be distributed widely throughout the L. polyphemus central nervous system. The visual system of L. polyphemus is now arguably the best understood among chelicerates, and as such, it is a critical resource for furthering our understanding of the evolution and diversification of visual systems in arthropods.