The unusual eyes of Xenos peckii (Strepsiptera: Xenidae) have green- and UV-sensitive photoreceptors

ABSTRACT The highly specialized evolution of Strepsiptera has produced one of the most unusual eyes among mature insects, perhaps in line with their extremely complex and challenging life cycle. This relatively rare insect order is one of the few for which it has been unclear what spectral classes of photoreceptors any of its members may possess, an even more apt question given the nocturnal evolution of the group. To address this question, we performed electroretinograms on adult male Xenos peckii: we measured spectral responses to equi-quantal monochromatic light flashes of different wavelengths, and established VlogI relationships to calculate spectral sensitivities. Based on opsin template fits, we found maximal spectral sensitivity (λmax) in the green domain at 539 nm. Application of a green light to ‘bleach’ green receptors revealed that a UV peak was contributed to by an independent UV opsin with a λmax of 346 nm. Transcriptomics and a phylogenetic analysis including 50 other opsin sequences further confirmed the presence of these two opsin classes. While these findings do not necessarily indicate that these unorthodox insects have color vision, they raise the possibility that UV vision plays an important role in the ability of X. peckii males to find the very cryptic strepsipteran females that are situated within their wasp hosts. Highlighted Article: Electroretinogram-based spectral response measurements suggest dichromacy in twisted-wing parasites.

[1]  Almut Kelber,et al.  Nocturnal colour vision – not as rare as we might think , 2006, Journal of Experimental Biology.

[2]  T. Cook,et al.  Spatial distribution of opsin-encoding mRNAs in the tiered larval retinas of the sunburst diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae) , 2009, Journal of Experimental Biology.

[3]  P. Skorupski,et al.  Photoreceptor Spectral Sensitivity in the Bumblebee, Bombus impatiens (Hymenoptera: Apidae) , 2010, PloS one.

[4]  P. Hargrave,et al.  Short wavelength-sensitive opsins from the Saharan silver and carpenter Ants , 1997, Invertebrate Neuroscience.

[5]  P. Hargrave,et al.  Ant opsins: Sequences from the Saharan silver ant and the carpenter ant , 1996, Invertebrate Neuroscience.

[6]  Jérôme Primot,et al.  Demonstration of an infrared microcamera inspired by Xenos peckii vision. , 2009, Applied optics.

[7]  J. Kathirithamby Review of the Order Strepsiptera , 1989 .

[8]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[9]  J. Kathirithamby,et al.  Atypical 'fibrillar' flight muscle in strepsiptera. , 1984, Tissue & cell.

[10]  R. Hoy,et al.  The unusual visual system of the Strepsiptera: external eye and neuropils , 2003, Journal of Comparative Physiology A.

[11]  N. P. Kristensen Phylogeny of Insect Orders , 1981 .

[12]  K. Donner,et al.  In search of the visual pigment template , 2000, Visual Neuroscience.

[13]  A. Kelber,et al.  Colour Vision: Parallel Pathways Intersect in Drosophila , 2013, Current Biology.

[14]  G. D. Bernard Red-Absorbing Visual Pigment of Butterflies , 1979, Science.

[15]  C. Trouth,et al.  Vision in the fireflyPhoturis lucicrescens (Coleoptera: Lampyridae): Spectral sensitivity and selective adaptation in the compound eye , 1982, Journal of comparative physiology.

[16]  C. Ballaré,et al.  A look into the invisible: ultraviolet-B sensitivity in an insect (Caliothrips phaseoli) revealed through a behavioural action spectrum , 2010, Proceedings of the Royal Society B: Biological Sciences.

[17]  T. Goldsmith,et al.  Behavior of crayfish rhodopsin and metarhodopsin in digitonin: the 510 and 562 nm “visual pigments” are artifacts , 1994, Vision Research.

[18]  Eric J. Warrant,et al.  Scotopic colour vision in nocturnal hawkmoths , 2002, Nature.

[19]  W. Smith,et al.  Opsins from the lateral eyes and ocelli of the horseshoe crab, Limulus polyphemus. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Armin Huber,et al.  Blue- and Green-Absorbing Visual Pigments ofDrosophila: Ectopic Expression and Physiological Characterization of the R8 Photoreceptor Cell-Specific Rh5 and Rh6 Rhodopsins , 1999, The Journal of Neuroscience.

[21]  N. Marshall,et al.  Ultraviolet polarisation sensitivity in the stomatopod crustacean Odontodactylus scyllarus , 2009, Journal of Comparative Physiology A.

[22]  K. Jeong,et al.  Ultrathin camera inspired by visual system of Xenos peckii , 2016, 2016 IEEE 29th International Conference on Micro Electro Mechanical Systems (MEMS).

[23]  Elke K Buschbeck,et al.  Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera) , 2007, Journal of Experimental Biology.

[24]  P. Towner,et al.  INVERTEBRATE VISUAL PIGMENTS , 1995, Photochemistry and photobiology.

[25]  T. Cronin,et al.  Short- and long-wavelength-sensitive opsins are involved in photoreception both in the retina and throughout the central nervous system of crayfish , 2015, Journal of Comparative Physiology.

[26]  David K Yeates,et al.  Single-copy nuclear genes resolve the phylogeny of the holometabolous insects , 2009, BMC Biology.

[27]  K. Crandall,et al.  Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. , 2006, Molecular biology and evolution.

[28]  M. Vorobyev,et al.  A review of the evolution of animal colour vision and visual communication signals , 2008, Vision Research.

[29]  U. Jahn,et al.  Stylopsal: The First Identified Female-produced Sex Pheromone of Strepsiptera , 2012, Journal of Chemical Ecology.

[30]  Martin Heisenberg,et al.  The rôle of retinula cell types in visual behavior ofDrosophila melanogaster , 2004, Journal of comparative physiology.

[31]  T. Wachtler,et al.  Color Discrimination with Broadband Photoreceptors , 2013, Current Biology.

[32]  G. Gries,et al.  New findings on life history traits of Xenos peckii (Strepsiptera: Xenidae) , 2014, The Canadian Entomologist.

[33]  T. Cronin,et al.  Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae) , 2000, Journal of Comparative Physiology A.

[34]  R. G. Foster,et al.  Two opsin genes from the vetch aphid, Megoura viciae , 2000, Insect molecular biology.

[35]  Samuel Rossel,et al.  Regional differences in photoreceptor performance in the eye of the praying mantis , 1979, Journal of comparative physiology.

[36]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[37]  Almut Kelber,et al.  Invertebrate colour vision , 2006 .

[38]  Eric J. Warrant,et al.  A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum , 2002, Journal of Comparative Physiology A.

[39]  R. Menzel,et al.  Spectral sensitivity of photoreceptors in insect compound eyes: Comparison of species and methods , 1986, Journal of Comparative Physiology A.

[40]  M. Vorobyev,et al.  Animal colour vision — behavioural tests and physiological concepts , 2003, Biological reviews of the Cambridge Philosophical Society.

[41]  J. Layne,et al.  Spectral sensitivity of the principal eyes of sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae), larvae , 2011, Journal of Experimental Biology.

[42]  D. Stavenga,et al.  Simple exponential functions describing the absorbance bands of visual pigment spectra , 1993, Vision Research.

[43]  Daiqin Li,et al.  It takes two peaks to tango: the importance of UVB and UVA in sexual signalling in jumping spiders , 2016, Animal Behaviour.

[44]  G. D. Bernard,et al.  Not all butterfly eyes are created equal: Rhodopsin absorption spectra, molecular identification, and localization of ultraviolet‐, blue‐, and green‐sensitive rhodopsin‐encoding mRNAs in the retina of Vanessa cardui , 2003, The Journal of comparative neurology.

[45]  N. Justin Marshall,et al.  Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans , 1989, Journal of Comparative Physiology A.

[46]  Tony Hunter,et al.  Microarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration , 2009, BMC Biology.

[47]  A. Briscoe,et al.  Six Opsins from the Butterfly Papilio glaucus: Molecular Phylogenetic Evidence for Paralogous Origins of Red-Sensitive Visual Pigments in Insects , 2000, Journal of Molecular Evolution.

[48]  S. Dötterl,et al.  First Sex Pheromone of the Order Strepsiptera: (3R,5R,9R)-3,5,9-Trimethyldodecanal in Stylops melittae Kirby, 1802 , 2012, Journal of Chemical Ecology.

[49]  W. Harris,et al.  Targeted misexpression of a Drosophila opsin gene leads to altered visual function , 1988, Nature.

[50]  T. Hariyama,et al.  A comparison of electrophysiologically determined spectral responses in 35 species of Lepidoptera , 1982 .

[51]  T. Ichikawa,et al.  Distribution of color receptors in the larval eyes of four species of lepidoptera , 2004, Journal of comparative physiology.

[52]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[53]  Richard H. White,et al.  Rhodopsins, retinula cell ultrastructure, and receptor potentials in the developing pupal eye of the mothManduca sexta , 1983, Journal of comparative physiology.

[54]  D. Hughes,et al.  Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures , 2003, Insectes Sociaux.

[55]  Elizabeth C. McDonald,et al.  Genomic and gene regulatory signatures of cryptozoic adaptation: Loss of blue sensitive photoreceptors through expansion of long wavelength-opsin expression in the red flour beetle Tribolium castaneum , 2007, Frontiers in Zoology.

[56]  J. Cook Review of the Biology of Parasitic Insects in the Order Strepsiptera , 2014 .

[57]  R. Beutel,et al.  The evolution of Strepsiptera (Hexapoda). , 2008, Zoology.

[58]  K Kirschfeld,et al.  Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  K. Naka,et al.  An attempt to analyse colour reception by electrophysiology , 1966, The Journal of physiology.

[60]  Claude Desplan,et al.  The Color-Vision Circuit in the Medulla of Drosophila , 2008, Current Biology.

[61]  R. Hoy,et al.  Chunk versus point sampling: visual imaging in a small insect. , 1999, Science.

[62]  L. Chittka,et al.  The evolution of color vision in insects. , 2001, Annual review of entomology.

[63]  N. Pierce,et al.  Honeybee Blue- and Ultraviolet-Sensitive Opsins: Cloning, Heterologous Expression in Drosophila, and Physiological Characterization , 1998, The Journal of Neuroscience.

[64]  Robert Leitel,et al.  Multi-aperture optics for wafer-level cameras , 2011 .

[65]  K. Arikawa,et al.  Pentachromatic visual system in a butterfly , 1987, Naturwissenschaften.

[66]  J. Zeil,et al.  Strepsipteran forewings are haltere-like organs of equilibrium , 1993, Naturwissenschaften.

[67]  A. Steiner,et al.  Spectral sensitivity ofCalliphora erythrocephala and other insect species studied with Fourier Interferometric Stimulation (FIS) , 1986, Journal of Comparative Physiology A.

[68]  T K Attwood,et al.  Fingerprinting G-protein-coupled receptors. , 1994, Protein engineering.

[69]  Erich Bornberg-Bauer,et al.  Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera , 2013, Current Biology.

[70]  Thomas Labhart,et al.  Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: Polarizational and angular sensitivity , 1980, Journal of comparative physiology.

[71]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[72]  Sakamoto,et al.  Two opsins from the compound eye of the crab Hemigrapsus sanguineus , 1996, The Journal of experimental biology.