Rhabdom evolution in butterflies: insights from the uniquely tiered and heterogeneous ommatidia of the Glacial Apollo butterfly,<i>Parnassius glacialis</i>

Matsushita, Atsuko; Awata, Hiroko; Wakakuwa, Motohiro; Takemura, Shin-ya; Arikawa, Kentaro

doi:10.1098/rspb.2012.0475

Cited by 17 publications

(13 citation statements)

References 48 publications

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“…This was to check whether the Troides eyes contained fluorescing ommatidia like in other Papilionid species [15], [19]. For the histological investigation of the retina, the compound eyes were isolated and fixed in 8% paraformaldehyde in 2% sodium cacodylate buffer (pH 7.4) at room temperature for 30 min, dehydrated in an acetone series and embedded in Epon resin.…”

Section: Methodsmentioning

confidence: 99%

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

2013

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The compound eye of the Golden Birdwing, Troides aeacus formosanus (Papilionidae, Lepidoptera), is furnished with three types of ommatidia, which are clearly different in pigmentation around the rhabdom. Each ommatidium contains nine photoreceptors, whose spectral sensitivities were analyzed electrophysiologically. We identified nine spectral types of photoreceptor with sensitivities peaking at 360 nm (UV), 390 nm (V), 440 nm (B), 510 nm (BG), 540 nm (sG), 550 nm (dG), 580 nm (O), 610 nm (R), and 630 nm (dR) respectively. The spectral sensitivities of the V, O, R and dR receptors did not match the predicted spectra of any visual pigments, but with the filtering effects of the pigments around the rhabdom, they can be reasonably explained. In some of the receptors, negative-going responses were observed when they were stimulated at certain wavelengths, indicating antagonistic interactions between photoreceptors.

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Section: Methodsmentioning

confidence: 99%

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

2013

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“…Another possible reason for the evolution of the tiered rhabdom is the establishment of a channel for motion vision, which the R3 and R4 green receptor system may represent, at least in Papilio and Pieris (Wakakuwa et al, 2007). However, the rhabdoms of L. amurensis exhibit little tiering (Figs3, 4), in common with many other insects including nymphalid butterflies (Gordon, 1977;Kolb, 1985;Matsushita et al, 2012), suggesting that the organization is ancestral (Matsushita et al, 2012).…”

Section: Evolutionary Viewmentioning

confidence: 99%

Rough eyes of the Northeast-Asian Wood White Leptidea amurensis

Uchiyama

Awata

Kinoshita

et al. 2013

Journal of Experimental Biology

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SUMMARYThe northeast-Asian wood white, Leptidea amurensis (Lepidoptera, Pieridae), belongs to the Dismorphiinae, a subfamily of the family Pieridae. We studied the structure of the compound eye in this species through a combination of anatomy, molecular biology and intracellular electrophysiology, with a particular focus on the evolution of butterfly eyes. We found that their eyes consist of three types of ommatidia, with a basic set of one short-, one middle-and one long-wavelength-absorbing visual pigment. The spectral sensitivities of the photoreceptors are rather simple, and peak in the ultraviolet, blue and green wavelength regions. The ommatidia have neither perirhabdomal nor fluorescent pigments, which modulate photoreceptor spectral sensitivities in a number of other butterfly species. These features are primitive, but the eyes of Leptidea exhibit another unique feature: the rough appearance of the ventral two-thirds of the eye. The roughness is due to the irregular distribution of facets of two distinct sizes. As this phenomenon exists only in males, it may represent a newly evolved sex-related feature.

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“…Papilio glaucus has eight visual opsins, six of which result from LW opsin duplications (Briscoe, 2000;Cong et al, 2015), while another papilionid, the birdwing Troides aeaca, has nine spectral classes of photoreceptor (Chen et al, 2013). Duplicated LW opsin genes are found in several species including a representative from the basal lineage of the family, Parnassius glacialis, suggesting the LW opsin duplication may have been present in the ancestral papilionid (Matsushita et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

McCulloch

Osorio

Briscoe

2016

Journal of Experimental Biology

122

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Most butterfly families expand the number of spectrally distinct photoreceptors in their compound eye by opsin gene duplications together with lateral filter pigments; however, most nymphalid genera have limited diversity, with only three or four spectral types of photoreceptor. Here, we examined the spatial pattern of opsin expression and photoreceptor spectral sensitivities in Heliconius erato, a nymphalid with duplicate ultraviolet opsin genes, UVRh1 and UVRh2. We found that the H. erato compound eye is sexually dimorphic. Females express the two UV opsin proteins in separate photoreceptors, but males do not express UVRh1. Intracellular recordings confirmed that females have three short wavelengthsensitive photoreceptors (λ max =356, ∼390 and 470 nm), while males have two (λ max =390 and ∼470 nm). We also found two long wavelength-sensitive photoreceptors (green, λ max ∼555 nm, and red, λ max ∼600 nm), which express the same LW opsin. The red cell's shifted sensitivity is probably due to perirhabdomal filtering pigments. Sexual dimorphism of the UV-absorbing rhodopsins may reflect the females' need to discriminate conspecifics from co-mimics. Red-green color vision may be used to detect differences in red coloration on Heliconius wings, or for host-plant identification. Among nymphalids so far investigated, only H. erato is known to possess five spectral classes of photoreceptor; sexual dimorphism of the eye via suppression of one class of opsin (here UVRh1 in males) has not -to our knowledge -been reported in any animal.

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Rhabdom evolution in butterflies: insights from the uniquely tiered and heterogeneous ommatidia of the Glacial Apollo butterfly,Parnassius glacialis

Cited by 17 publications

References 48 publications

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

Rough eyes of the Northeast-Asian Wood White Leptidea amurensis

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

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