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. 2017 Nov 29:11:96.
doi: 10.3389/fncir.2017.00096. eCollection 2017.

Unique Temporal Expression of Triplicated Long-Wavelength Opsins in Developing Butterfly Eyes

Kentaro Arikawa  1 , Tomoyuki Iwanaga  2 , Motohiro Wakakuwa  1 , Michiyo Kinoshita  1
Affiliations

Unique Temporal Expression of Triplicated Long-Wavelength Opsins in Developing Butterfly Eyes

Kentaro Arikawa et al. Front Neural Circuits. .

Abstract

Following gene duplication events, the expression patterns of the resulting gene copies can often diverge both spatially and temporally. Here we report on gene duplicates that are expressed in distinct but overlapping patterns, and which exhibit temporally divergent expression. Butterflies have sophisticated color vision and spectrally complex eyes, typically with three types of heterogeneous ommatidia. The eyes of the butterfly Papilio xuthus express two green- and one red-absorbing visual pigment, which came about via gene duplication events, in addition to one ultraviolet (UV)- and one blue-absorbing visual pigment. We localized mRNAs encoding opsins of these visual pigments in developing eye disks throughout the pupal stage. The mRNAs of the UV and blue opsin are expressed early in pupal development (pd), specifying the type of the ommatidium in which they appear. Red sensitive photoreceptors first express a green opsin mRNA, which is replaced later by the red opsin mRNA. Broadband photoreceptors (that coexpress the green and red opsins) first express the green opsin mRNA, later change to red opsin mRNA and finally re-express the green opsin mRNA in addition to the red mRNA. Such a unique temporal and spatial expression pattern of opsin mRNAs may reflect the evolution of visual pigments and provide clues toward understanding how the spectrally complex eyes of butterflies evolved.

Keywords: compound eye; development; eye disk; insect; ommatidium; photoreceptor; rhodopsin; visual pigment.

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Figures

Figure 1
Figure 1
Butterfly ommatidia. (A) Diagram of a tiered ommatidium. Nine photoreceptors (1–9) form a phototransductive rhabdom along the central axis. (B) Transverse section of distal rhabdom of adult. (C) Insect phylogeny and photoreceptor number per ommatidium. Right diagrams show typical ommatidial types. (D) Three ommatidial types of Papilio xuthus. Information about pR9 photoreceptors is limited, but see also Figure 5 in Briscoe (2008) for opsins expressed in the pR9 cells of Papilio glaucus. Ss, Spineless; S(λ), spectral sensitivity.
Figure 2
Figure 2
Developing compound eyes of Papilio xuthus in day 2 (A–C), day 5 (D–F) and day 8 (G–I) pupae. General appearance of the eye disk in the pupa (A,D,G), and the longitudinal (B,E,H) and transverse (C,F,I) sections. Scales = 50 μm.
Figure 3
Figure 3
Electron micrographs of developing rhabdom in the eye disk from pupae. (A) Day 1. Eight columnar cells (*) and flat cells (**) are evident. (B) Day 2. Membrane of photoreceptor precursors start evaginating (black arrowheads). White arrowheads indicate desmosome-like junctions. (C) Day 4. Arrowheads indicate interphotoreceptor junctions as in adult ommatidia (see Figure 1B). (D) Day 5. Interphotoreceptor spaces enlarge (arrowheads). (E) Day 7. (F) Day 9. Scales = 2 μm.
Figure 4
Figure 4
Expression analysis of five visual pigment opsins by RT-PCR. Numbers on the top indicate days after pupation, and A for adult. As a control, the actin cDNA is amplified.
Figure 5
Figure 5
Histological in situ hybridization of five opsin mRNAs in the developing and adult compound eyes of Papilio xuthus. (A–C) PxUV. (D–F) PxB. (G–I) PxG1. (J–N) PxG2. (O–R) PxR. Developmental stages are indicated in each pictures. Three framed pairs are from adjacent sections labeled with different probes. Solid, broken and dotted circles indicate type I, II and III ommatidia. Arrowheads in (K) indicate six cells labeled. Scales = 20 μm.
Figure 6
Figure 6
Development of the Papilio pupal eye disk.
Figure 7
Figure 7
Summary diagram of the in situ hybridization results of day 5 and day 7 pupae with the final state in the adult.
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References

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