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The Giant Butterfly-Moth Paysandisia Archon Has Spectrally Rich University of Groningen The giant butterfly-moth Paysandisia archon has spectrally rich apposition eyes with unique light-dependent photoreceptor dynamics Pirih, Primoz; Ilić, Marko; Rudolf, Jerneja; Arikawa, Kentaro; Stavenga, Doekele; Belušič, Gregor Published in: Journal of Comparative Physiology A DOI: 10.1007/s00359-018-1267-z IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2018 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Pirih, P., Ilić, M., Rudolf, J., Arikawa, K., Stavenga, D., & Belušič, G. (2018). The giant butterfly-moth Paysandisia archon has spectrally rich apposition eyes with unique light-dependent photoreceptor dynamics. Journal of Comparative Physiology A, 204(7), 639-651. https://doi.org/10.1007/s00359-018- 1267-z Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license. More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne- amendment. Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Journal of Comparative Physiology A (2018) 204:639–651 https://doi.org/10.1007/s00359-018-1267-z ORIGINAL PAPER The giant butterfly-moth Paysandisia archon has spectrally rich apposition eyes with unique light-dependent photoreceptor dynamics Primož Pirih1,2 · Marko Ilić3 · Jerneja Rudolf3,4 · Kentaro Arikawa1 · Doekele G. Stavenga5 · Gregor Belušič3 Received: 3 December 2017 / Revised: 20 April 2018 / Accepted: 16 May 2018 / Published online: 4 June 2018 © The Author(s) 2018 Abstract The palm borer moth Paysandisia archon (Burmeister, 1880) (fam. Castniidae) is a large, diurnally active palm pest. Its compound eyes consist of ~ 20,000 ommatidia and have apposition optics with interommatidial angles below 1°. The omma- tidia contain nine photoreceptor cells and appear structurally similar to those in nymphalid butterflies. Two morphological ommatidial types were identified. Using the butterfly numbering scheme, in type I ommatidia, the distal rhabdom consists exclusively of the rhabdomeres of photoreceptors R1–2; the medial rhabdom has contributions from R1–8. The rhabdom in type II ommatidia is distally split into two sub-rhabdoms, with contributions from photoreceptors R2, R3, R5, R6 and R1, R4, R7, R8, respectively; medially, only R3–8 and not R1–2 contribute to the fused rhabdom. In both types, the pigmented bilobed photoreceptors R9 contribute to the rhabdom basally. Their nuclei reside in one of the lobes. Upon light adaptation, in both ommatidial types, the rhabdoms secede from the crystalline cones and pigment granules invade the gap. Intracellular recordings identified four photoreceptor classes with peak sensitivities in the ultraviolet, blue, green and orange wavelength regions (at 360, 465, 550, 580 nm, respectively). We discuss the eye morphology and optics, the photoreceptor spectral sensitivities, and the adaptation to daytime activity from a phylogenetic perspective. Keywords Palm borer moth · Compound eye · Spectral sensitivity · Lepidoptera · Phylogeny Introduction Electronic supplementary material The online version of this The palm borer moth Paysandisia archon (Burmeister, 1880) article (https ://doi.org/10.1007/s0035 9-018-1267-z) contains (Lepidoptera: Castniidae) is a large moth native to Uruguay supplementary material, which is available to authorized users. and Argentina. Its caterpillars live in galleries in palm tree * Primož Pirih trunks. The recent introduction to Europe has had a devastat- [email protected] ing effect on the decorative palm trees around the Mediter- ranean Sea and may potentially cause severe problems to the 1 Department of Evolutionary Studies of Biosystems, date production in North Africa and the Levant. The adult SOKENDAI The Graduate University for Advanced Studies, Paysandisia Shonan International Village, Hayama 240-0115, Kanagawa, male and female are diurnally active (Sarto i Japan Monteys et al. 2016; Frérot et al. 2017). The male emits 2 Department of Artificial Intelligence, University short-range pheromones and is territorial. As the female of Groningen, Nijenborgh 9, 9747 AG Groningen, probably does not produce long-range pheromones, to initi- The Netherlands ate mating, a male must first see a female before it starts 3 Department of Biology, Biotechnical faculty, University displaying its colours at close range, suggesting that the of Ljubljana, Večna pot 111, 1000 Ljubljana, Slovenia large compound eyes play an important role in intraspecific 4 Sars International Centre for Marine Molecular Biology, recognition (Sarto i Monteys et al. 2012; Frérot et al. 2013; University of Bergen, Thormøhlensgt. 55, 5006 Bergen, Quero et al. 2017; review: Sarto i Monteys et al. 2016). Norway The compound eyes of Paysandisia have a conspicuous 5 Department of Computational Physics, Zernike Institute pattern of pseudopupils, resembling the pseudopupil pattern for Advanced Materials, University of Groningen, Nijenborgh of the apposition eyes of pierid and nymphalid butterflies 4, NL, 9747AG Groningen, The Netherlands Vol.:(0123456789)1 3 640 Journal of Comparative Physiology A (2018) 204:639–651 (Stavenga 1979), thus indicating that also Paysandisia has et al. 1979; Meinecke and Langer 1984) and in the corn apposition eyes. Paysandisia belongs to the family Cast- borer moth Ostrinia (Crambidae) by intracellular recordings niidae, part of the superfamily Cossioidea, which groups (Belušič et al. 2017). To our knowledge, there are no func- together with Zygaenidae (burnets). The two superfamilies tional studies of the visual system in apodytrisian moths, so are placed in the clade Apodytrisia, either just outside or in one has to rely on the interpretations of earlier collections the beginning of the subclade Obtectomera (Mutanen et al. of histological data (e.g. Ehnbom 1948; Tuurala 1954; Yagi 2010; Heikkilä et al. 2015; Mitter et al. 2017). The day- and Koyama 1963). flying apodytrisian moths have apposition eyes, e.g. mem- The structural and functional aspects of butterfly (papil- bers of the families Sesiidae (Eby et al. 2013), Epicopeiidae ionoid) eyes have been studied extensively. The emerging and Zygaenidae (Yagi and Koyama 1963). In the order of comparative picture is that butterfly compound eyes have Lepidoptera, however, the majority of species is nocturnally three ommatidial types, with each ommatidium containing active. Their superposition eyes provide a higher sensitivity nine photoreceptor (retinula) cells (Arikawa and Stavenga in low-light conditions (Land and Nilsson 2012). A recent 1997; Qiu et al. 2002; Ogawa et al. 2013; Chen et al. 2016; comparative morphological study of the microlepidopteran reviewed by: Stavenga and Arikawa 2006; Arikawa 2017). families basal to Apodytrisia has postulated an intermedi- The butterfly (B) numbering scheme maps to the dipteran ate eye morphology as an adaptation of minute-sized eyes (D) numbering scheme in the following manner: B1–2 → to nocturnal activity (Fischer et al. 2012, 2014). A similar D7, B3–8 → D1–6, B9 → D8 (Friedrich et al. 2011; Ari- morphology where the proximal rhabdom is thick, while the kawa 2017). The number of spectral receptor classes varies thin distal rhabdoms reach the dioptric apparatus, has also among different butterfly species. Intracellular recordings in been confirmed with ultrastructure in comparatively larger some nymphalids identified a basic set of spectral receptors eyes of some moth families, e.g. in Tortricidae (Satoh et al. with three visual pigments (Kinoshita et al. 1997), which 2017), Pyralidae (Horridge and Giddings 1971) and Cram- appears to be based on three opsins (Briscoe et al. 2003; bidae (Belušič et al. 2017) and may be present in some other Briscoe and Bernard 2005). The photoreceptor spectral groups (Yagi and Koyama 1963). Most “true butterflies”, sensitivities can be modified by multiple opsin expression the Papilionoidea, have apposition eyes with thin rhab- in one cell (Kitamoto et al. 1998; Ogawa et al. 2012) and doms, with the exception of the diurnal Hesperiidae (Hor- by screening pigments acting as spectral filters (Arikawa ridge et al. 1972; Shimohigashi and Tominaga 1986) and et al. 1999; Stavenga et al. 2001; Stavenga 2002; Qiu et al. nocturnal Hedylidae (Yack et al. 2007), which both have 2002; Zaccardi et al. 2006; Stavenga and Arikawa 2011). superposition eyes. The papilionoid Papilio xuthus employs both mechanisms A requirement of the superposition eye design is that the and appears to have five opsins that serve as the basis for dioptric apparatus has afocal (telescopic) optics (Nilsson six spectral receptor classes (Arikawa 2017). The modifica- 1989). The
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