Spectral organization of ommatidia in flower-visiting insects.

This article reviews recent advances of studies on the spectral organization of the compound eye in lepidopteran and hymenopteran insects. The compound eyes consist of ommatidia, which contain a set of photoreceptor cells. The common feature is that the ommatidia can be divided into three types, according to the combination of spectral classes of photoreceptors. Honeybees and nymphalid butterflies provide the simplest case with three photoreceptor classes having peak sensitivities in the ultraviolet (UV), blue (B), or green (G) wavelength region. These receptors populate the ommatidia in fixed combinations. In type I ommatidia, the main eight photoreceptors consist of one UV, one B, and six G receptors. Type II has two UV and six G receptors, and type III has two B and six G receptors. The organization is basically retained in all insect species studied so far, although some butterflies have more than six classes of spectral receptors, including those sensitive in the violet and red wavelength regions. To acquire these additional receptors, two distinct strategies are applied: the multiple opsin strategy, taken by the Japanese yellow swallowtail butterfly Papilio xuthus, and the filter strategy, used by the small white butterfly Pieris rapae.

Wakakuwa M ，Stavenga DG ，Arikawa K 《PHOTOCHEMISTRY AND PHOTOBIOLOGY》

Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus.

The compound eye of the butterfly Papilio xuthus is composed of three types of spectrally heterogeneous ommatidia. The ommatidia, which contain nine photoreceptor cells, R1-9, bear four (type I), three (type II), or two (type III) classes of spectral receptors in fixed combinations. The photoreceptors send their axons to the lamina, the first optic ganglion, where the R1-9 axons originating from a single ommatidium, together with some second-order neurons, form a neuronal bundle, called a lamina cartridge. We investigated the axonal structure of photoreceptors in the lamina to determine whether the cartridge structure is different between the three ommatidial types. We first characterized a photoreceptor by measuring its spectral sensitivity and then injected Lucifer Yellow. We subsequently identified the type of ommatidium of the injected photoreceptor via histological sections. We further observed the axonal structure of the photoreceptor in the lamina by laser confocal microscopy. We found that the number and length of axon collaterals markedly differ between the spectral receptors. Those having the most extensive axon collaterals, which extend into six or more surrounding cartridges, are violet receptors (R1 and R2 of type II ommatidia). UV receptors (R1 or R2 of type I ommatidia) also send collaterals into two to four neighboring cartridges. Blue receptors (R1 or R2 of type I ommatidia, R1 and R2 of type III ommatidia) have short collaterals restricted to their own cartridges. We thus conclude that the neuronal circuit of the lamina cartridge differs between the three types of ommatidia.

Takemura SY ，Kinoshita M ，Arikawa K 《JOURNAL OF COMPARATIVE NEUROLOGY》

Spectral organization of the eye of a butterfly, Papilio.

This review outlines our recent studies on the spectral organization of butterfly compound eyes, with emphasis on the Japanese yellow swallowtail butterfly, Papilio xuthus, which is the most extensively studied species. Papilio has color vision when searching for nectar among flowers, and their compound eyes are furnished with six distinct classes of spectral receptors (UV, violet, blue, green, red, broadband). The compound eyes consist of many ommatidia, each containing nine photoreceptor cells. How are the six classes of spectral receptors arranged in the ommatidia? By studying their electrophysiology, histology, and molecular biology, it was found that the Papilio ommatidia can be divided into three types according to the combination of spectral receptors they contain. Different types of ommatidia are distributed randomly over the retina. Histologically, the heterogeneity appeared to be related to red or yellow pigmentation around the rhabdom. A subset of red-pigmented ommatidia contains 3-hydroxyretinol in the distal portion, fluorescing under UV epi-illumination. The red, yellow and fluorescing pigments all play crucial roles in determining the spectral sensitivities of receptors. Spectral heterogeneity and random array of ommatidia have also been found in other lepidopteran species. Similarities and differences between species are also discussed.

Arikawa K 《JOURNAL OF COMPARATIVE PHYSIOLOGY A-NEUROETHOLOGY SENSORY NEURAL AND BEHAVIORAL PHYSIOLOGY》

Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus.

The compound eye of the butterfly Papilio xuthus is composed of three spectrally distinct types of ommatidia. We investigated the blue and double-peaked green receptors that are encountered distally in type I and III ommatidia, by means of intracellular recordings, in vivo fluorescence microscopy, and histology. The blue receptors are R1 and/or R2 photoreceptors; they contain the same mRNA encoding the opsin of the blue-absorbing visual pigment. However, here we found that the sensitivity in the UV wavelength region strongly depends on the ommatidial type; the blue receptors in type I ommatidia have a distinctly depressed UV sensitivity, which is attributed to lateral filtering in the fused rhabdom. In the main, fronto-ventral part of the eye, the R3 and R4 photoreceptors of all ommatidia contain the same set of two mRNAs encoding the opsins of green-absorbing visual pigments, PxL1 and PxL2. The spectral sensitivities are double-peaked, but the UV sensitivity of the R3 and R4 photoreceptors in type I ommatidia appears to be reduced, similar to that of the co-localized blue receptors.

Kinoshita M ，Kurihara D ，Tsutaya A ，Arikawa K ... -  《ZOOLOGICAL SCIENCE》

Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus.

The eye of the butterfly Papilio xuthus contains a random array of three types of ommatidia (types I-III), each bearing nine photoreceptors, R1-R9. Of the six spectral classes of photoreceptors identified, types I, II, and III ommatidia contain four, three, and two classes, respectively: the ommatidia are thus spectrally heterogeneous. The photoreceptors send their axons to the lamina where, together with some large monopolar cells (LMCs), the nine from a single ommatidium contribute to a module called a lamina cartridge. We recently reported that among different photoreceptor axon terminals visualized by confocal microscopy, the number and length of axon collaterals differ for different spectral receptors, suggesting that lamina circuits are specific for each ommatidial type. Here we studied the distribution of synapse-like structures in the cartridges, first characterizing a photoreceptor by measuring its spectral sensitivity and then injecting Lucifer yellow (LY). We subsequently histologically identified the type of ommatidium to which the injected photoreceptor belonged, cut serial ultrathin sections of the entire lamina, labeled these with anti-LY immunocytochemistry, and then localized synapse-like structures. We found numerous interphotoreceptor contacts both within and between cartridges, the combination of which was again specific for the ommatidial type. R3 and R4, which are green-sensitive photoreceptors in all ommatidia, have thick axons lacking collaterals. We found that these cells exclusively make contacts with LMCs and not with photoreceptors. We therefore presume that R3 and R4 construct a system for motion vision, whereas other randomly distributed spectral types provide inputs for color vision.

Takemura SY ，Arikawa K 《JOURNAL OF COMPARATIVE NEUROLOGY》