Pancrustacea (Hexapoda plus Crustacea) display an enormous diversity of eye designs, including multiple types of compound eyes and single-chambered eyes, often with color vision and/or polarization vision. Although the eyes of some pancrustaceans are well-studied, there is still much to learn about the evolutionary paths to this amazing visual diversity. Here, we examine the evolutionary history of eyes and opsins across the principle groups of Pancrustacea. First, we review the distribution of lateral and median eyes, which are found in all major pancrustacean clades (Oligostraca, Multicrustacea, and Allotriocarida). At the same time, each of those three clades has taxa that lack lateral and/or median eyes. We then compile data on the expression of visual r-opsins (rhabdomeric opsins) in lateral and median eyes across Pancrustacea and find no evidence for ancient opsin clades expressed in only one type of eye. Instead, opsin clades with eye-specific expression are products of recent gene duplications, indicating a dynamic past, during which opsins often changed expression from one type of eye to another. We also investigate the evolutionary history of peropsins and r-opsins, which are both known to be expressed in eyes of arthropods. By searching published transcriptomes, we discover for the first time crustacean peropsins and suggest that previously reported odonate opsins may also be peropsins. Finally, from analyzing a reconciled, phylogenetic tree of arthropod r-opsins, we infer that the ancestral pancrustacean had four visual opsin genes, which we call LW2, MW1, MW2, and SW. These are the progenitors of opsin clades that later were variously duplicated or lost during pancrustacean evolution. Together, our results reveal a particularly dynamic history, with losses of eyes, duplication and loss of opsin genes, and changes in opsin expression between types of eyes.

Many insects exploit skylight polarization as a compass cue for orientation and navigation. In the fruit fly, Drosophila melanogaster, photoreceptors R7 and R8 in the dorsal rim area (DRA) of the compound eye are specialized to detect the electric vector (e-vector) of linearly polarized light. These photoreceptors are arranged in stacked pairs with identical fields of view and spectral sensitivities, but mutually orthogonal microvillar orientations. As in larger flies, we found that the microvillar orientation of the distal photoreceptor R7 changes in a fan-like fashion along the DRA. This anatomical arrangement suggests that the DRA constitutes a detector for skylight polarization, in which different e-vectors maximally excite different positions in the array. To test our hypothesis, we measured responses to polarized light of varying e-vector angles in the terminals of R7/8 cells using genetically encoded calcium indicators. Our data confirm a progression of preferred e-vector angles from anterior to posterior in the DRA, and a strict orthogonality between the e-vector preferences of paired R7/8 cells. We observed decreased activity in photoreceptors in response to flashes of light polarized orthogonally to their preferred e-vector angle, suggesting reciprocal inhibition between photoreceptors in the same medullar column, which may serve to increase polarization contrast. Together, our results indicate that the polarization-vision system relies on a spatial map of preferred e-vector angles at the earliest stage of sensory processing.

Multiple visual pigments, prerequisites for color vision, are found in arthropods, but the evolutionary origin of their diversity remains obscure. In this study, we explore the opsin genes in five distantly related species of Onychophora, using deep transcriptome sequencing and screening approaches. Surprisingly, our data reveal the presence of only one opsin gene (onychopsin) in each onychophoran species, and our behavioral experiments indicate a maximum sensitivity of onychopsin to blue-green light. In our phylogenetic analyses, the onychopsins represent the sister group to the monophyletic clade of visual r-opsins of arthropods. These results concur with phylogenomic support for the sister-group status of the Onychophora and Arthropoda and provide evidence for monochromatic vision in velvet worms and in the last common ancestor of Onychophora and Arthropoda. We conclude that the diversification of visual pigments and color vision evolved in arthropods, along with the evolution of compound eyes-one of the most sophisticated visual systems known.

BackgroundOpsins are key proteins in animal photoreception. Together with a light-sensitive group, the chromophore, they form visual pigments which initiate the visual transduction cascade when photoactivated. The spectral absorption properties of visual pigments are mainly determined by their opsins, and thus opsins are crucial for understanding the adaptations of animal eyes. Studies on the phylogeny and expression pattern of opsins have received considerable attention, but our knowledge about insect visual opsins is still limited. Up to now, researchers have focused on holometabolous insects, while general conclusions require sampling from a broader range of taxa. We have therefore investigated visual opsins in the ocelli and compound eyes of the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect.ResultsPhylogenetic analyses place all identified cricket sequences within the three main visual opsin clades of insects. We assign three of these opsins to visual pigments found in the compound eyes with peak absorbances in the green (515 nm), blue (445 nm) and UV (332 nm) spectral range. Their expression pattern divides the retina into distinct regions: (1) the polarization-sensitive dorsal rim area with blue- and UV-opsin, (2) a newly-discovered ventral band of ommatidia with blue- and green-opsin and (3) the remainder of the compound eye with UV- and green-opsin. In addition, we provide evidence for two ocellar photopigments with peak absorbances in the green (511 nm) and UV (350 nm) spectral range, and with opsins that differ from those expressed in the compound eyes.ConclusionsOur data show that cricket eyes are spectrally more specialized than has previously been assumed, suggesting that similar adaptations in other insect species might have been overlooked. The arrangement of spectral receptor types within some ommatidia of the cricket compound eyes differs from the generally accepted pattern found in holometabolous insect taxa and awaits a functional explanation. From the opsin phylogeny, we conclude that gene duplications, which permitted differential opsin expression in insect ocelli and compound eyes, occurred independently in several insect lineages and are recent compared to the origin of the eyes themselves.