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All the better to see you with: a review of odonate color vision with transcriptomic insight into the odonate eye

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Abstract

Although dragonflies and damselflies (Insecta: Odonata) represent some of the most advanced visual systems among insects, odonate visual systems are not as well understood as those of model or more economically important insects. Yet, with their large and complex eyes, aquatic and terrestrial life stages, entirely carnivorous lifestyle, exceptional mating behaviors, diversity in coloration, occupancy of diverse light environments, and adult success that is completely dependent on vision, it would seem studying the visual system of Odonata at the molecular level would yield highly rewarding scientific findings related to predator/prey interactions, the physiological and molecular shifts associated with ecological shifts in light environments, and the role of vision on behavioral ecology. Here, we provide a review of odonate color vision. The first odonate opsin sequences are published using a degenerate PCR approach for both dragonfly and damselfly lineages as well as a transcriptome approach for a single species of damselfly. These genetic data are combined with electrophysiology data from odonates to examine genotype/phenotype relationships in this visual system. Using these data, we present the first insights into the evolution and distribution of the visual pigments (opsins) among odonates. The integration of molecular and behavioral studies of odonate vision will help answer long-standing questions about how sensory systems and coloration may coevolve.

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References

  • Anderson, C. N., & Grether, G. F. (2009). Interspecific aggression and character displacement of competitor recognition in Hetaerina damselflies. Proceedings of the Royal Society B, 277, 549–555.

    Article  PubMed  Google Scholar 

  • Armett-Kibel, C., & Menertzhagen, I. A. (1983). Structural organization of the ommatidium in the ventral compound eye of the dragonfly Sympetrum. Journal of Comparative Physiology A, 151, 285–294.

    Article  Google Scholar 

  • Briscoe, A. D., & Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology, 46, 471–510.

    Article  PubMed  CAS  Google Scholar 

  • Briscoe, A. D., Bybee, S. M., Bernard, G. D., Yuan, F., Sison-Mangus, M. P., Reed, R. D., et al. (2010). Positive selection of a duplicated ultraviolet-sensitive visual pigment coincides with wing pigment evolution in Heliconius butterflies. Proceedings of the National Academy of Sciences, U.S.A., 107, 3628–3633.

    Article  Google Scholar 

  • Bybee, S. M., Ogden, T. H., Branham, M. A., & Whiting, M. F. (2008). Molecules, morphology and fossils: A comprehensive approach to odonate phylogeny and the evolution of the odonate wing. Cladistics, 24, 477–514.

    Article  Google Scholar 

  • Bybee, S. M., Yuan, F., Ramstetter, M. D., Llorente-Bousquets, J., Reed, R. D., Osorio, D., et al. (2012). UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication. The American Naturalist, 179, 38–51.

    Article  PubMed  Google Scholar 

  • Chang, B. S. W., Crandall, K. A., Carulli, J. P., & Hartl, D. L. (1995). Opsin phylogeny and evolution: A model for blue shifts in wavelength regulation. Molecular Phylogenetics and Evolution, 4, 31–43.

    Article  PubMed  CAS  Google Scholar 

  • Chittka, L. (1997). Bee color vision is optimal for coding flower colors, but flower colors are not optimal for being coded—why? Israeli Journal of Plant Science, 45, 115–127.

    Google Scholar 

  • Clement, S. L., & Meyer, R. P. (1980). Adult biology and behavior of the dragonfly Tanypteryx hageni (Odonata: Petaluridae). Journal of the Kansas Entomological Society, 53, 711–719.

    Google Scholar 

  • Cooper, I. A. (2010). Ecology of sexual dimorphism and clinal variation of coloration in a damselfly. The American Naturalist, 176(5), 566–572.

    Article  PubMed  Google Scholar 

  • Corbet, P. (1999). Dragonflies: Behavior and ecology of Odonata. Ithaca: Cornell University Press.

    Google Scholar 

  • Cordero, A. (1991). Fecundity of Ischnura graellsii (Rambur) in the laboratory (Odonata: Coenagrionidae). Odonatologica, 20(1), 37–44.

    Google Scholar 

  • Cronin, T. W., Jarvilehto, M., Weckstrom, M., & Lall, A. B. (2000). Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). Journal of Comparative Physiology A, 186, 1–12.

    Article  CAS  Google Scholar 

  • Cummings, M. E. (2004). Modelling divergence in luminance and chromatic detection performance across measured divergence in surfperch (Embiotocidae) habitats. Vision Research, 44(11), 1127–1145.

    Article  PubMed  Google Scholar 

  • Defrize, J., Théry, M., & Casas, J. (2010). Background colour matching by a crab spider in the field: A community sensory ecology perspective. The Journal of Experimental Biology, 213, 1425–1435.

    Article  PubMed  Google Scholar 

  • Endler, J. A. (1993). The color of light in forests and its implications. Ecological. Monographs, 63, 1–27.

    Article  Google Scholar 

  • Fincke, O. M. (1987). Female monogamy in the damselfly Ischnura verticalis Say (Zygoptera: Coenagrionidae). Odonatologica, 16, 129–143.

    Google Scholar 

  • Fincke, O. M. (2004). Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Animal Behavior, 67, 833–845.

    Article  Google Scholar 

  • Fincke, O. M., Jödicke, R., Paulson, D., & Schultz, D. T. (2005). The evolution and frequency of female color morphs in Holarctic Odonata: Why are male-like morphs typically the minority? International Journal of Odonatology, 8, 183–212.

    Article  Google Scholar 

  • Forbes, M. (1994). Tests of hypotheses for female-limited polymorphism in the damselfly, Enallagma boreale Selys. Animal Behaviour, 47, 742–726.

    Article  Google Scholar 

  • Fuller, R. C., Noa, L. A., & Strellner, R. S. (2010). Teasing apart the many effects of lighting environment on Opsin expression and foraging preference in bluefin killifish. American Naturalist, 176(1), 1–13.

    Article  PubMed  Google Scholar 

  • Gorb, S. N. (1998). Visual cues in mate recognition by males of the damselfly, Coenagrion puella (L.) (Odonata: Coenagrionidae). Journal of Insect Behavior, 11(1), 73–92.

    Article  Google Scholar 

  • Hardie, R. C. (1986). The photoreceptor array of the dipteran retina. Trends in Neuroscience, 9, 419–23.

    Article  Google Scholar 

  • Hariyama, T., Ozaki, K., Tokunaga, F., & Tsukahara, Y. (1993). Primary structure of crayfish visual pigment deduced from cDNA. FEBS Letters, 315(3), 287–292.

    Article  PubMed  CAS  Google Scholar 

  • Hisada, M., Tamasige, M., & Suzuki, N. (1965). Control of the flight of the dragonfly Sympetrum darwinianum Selys I. Dorsophotic response. Journal of the Faculty of Science Hokkaido University, Series 6, Zoology, 15, 568–577.

    Google Scholar 

  • Horridge, G. A. (1969). Unit studies on the retina of dragonflies. Zeitschrift fur Vergleichende Physiologie, 62, 1–37.

    Article  Google Scholar 

  • Iserbyt, A., & Van Gossum, H. (2011). Show your true colour: Cues for male mate preference in an intra-specific mimicry system. Ecological Entomology, 36, 544–548.

    Article  Google Scholar 

  • Janananda, B. G. (2011). Characterization of changes in Megalagrion opsin genes to detect signatures of selection. Open Access Theses. Paper 259.

  • Kaiser, H. (1985). Availability of receptive females at the mating place and mating chances of males in the dragonfly Aeschna cyanea. Behavioral Ecology and Sociobiology, 18(1), 1–7.

    Google Scholar 

  • Kirschfeld, K. (1976). The resolution of lens and compound eyes. In F. Zettler & R. Weiler (Eds.), Neural principles in vision (pp. 354–370). Springer: Berlin.

    Chapter  Google Scholar 

  • Land, M. F. (1981). Optics and vision in invertebrates. In H. Autrum (Ed.), Handbook of sensory physiology, Vol. VII/6B (pp. 471–592). Berlin: Springer.

    Google Scholar 

  • Land, M. F. (1989). Variations in the structure and design of compound eyes. In D. G. Stavenga & R. C. Hardie (Eds.), Facets of vision (pp. 90–111). Berlin: Springer-Verlag.

    Chapter  Google Scholar 

  • Land, M. F., & Nilsson, D. E. (2002). Animal eyes. Oxford: Oxford University Press.

    Google Scholar 

  • Laughlin, S. B. (1976). The sensitivities of dragonfly photoreceptors and the voltage gain of transduction. Journal of Comparative Physiology, 111, 221–247.

    Article  Google Scholar 

  • Lavoie-Dornik, J., Pilon, J.-G., Gogala, M., & Ali, M. A. (1988). Electrophysiological study of compound eye growth in Enallagma cyathigerum Charpentier and Enallagma clausum Morse Zygotpera Coenagrionidae. Odonatologica, 17(4), 337–356.

    Google Scholar 

  • Lythgoe, J. N. (1972). The adaptation of visual pigments to the photic environment. In H. Dartnall (Ed.), Handbook of sensory physiology, vol. 7, part 1: Photochemistry of vision (pp. 566–603). Berlin: Springer-Verlag.

    Google Scholar 

  • Maksimovic, S., Cook, T. A., & Buschbeck, E. K. (2009). Spatial distribution of opsin-encoding mRNAs in the tiered larval retinas of the sunburst diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae). Journal of Experimental Biology, 212(23), 3781–3794.

    Article  PubMed  CAS  Google Scholar 

  • Maksimovic, S., Layne, J. E., & Buschbeck, E. K. (2011). Spectral sensitivity of the principal eyes of sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae), larvae. Journal of Experimental Biology, 214(21), 3524–3531.

    Article  PubMed  Google Scholar 

  • Mayer, E. P., & Labhart, T. (1993). Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselflies (Odonata). Cell & Tissue Research, 272, 17–22.

    Article  Google Scholar 

  • Meinertzhagen, I. A., Menzel, R., & Kahle, G. (1983). The identification of spectral receptor types in the retina and lamina of the dragonfly Sympetrum rebicundulum. Journal of Comparative Physiology, 151, 295–310.

    Article  Google Scholar 

  • Morehouse, N. I., & Rutowski, R. L. (2010). In the eyes of the beholders: Female choice and avian predation risk associated with an exaggerated male butterfly color. American Naturalist, 176, 768–784.

    Article  PubMed  Google Scholar 

  • Nilsson, D.-E. (1989). Optics and evolution of the compound eye. In D. G. Stavenga & R. Hardie (Eds.), Facets of vision. Berlin: Springer.

    Google Scholar 

  • Nilsson, D.-E., & Kelber, A. (2007). A functional analysis of compound eye evolution. Arthropod Structure & Development, 36, 373–385.

    Article  Google Scholar 

  • Olberg, R. M., Worthington, A. H., & Venator, K. R. (2000). Prey pursuit and interception in dragonflies. Journal of Comparative Physiology A, 186, 155–162.

    Article  CAS  Google Scholar 

  • Olberg, R. M., Worthington, A. H., Fox, J. L., Bessette, C. E., & Loosemore, M. P. (2005). Prey size selection and distance estimation in foraging adult dragonflies. Journal of Comparative Physiology A, 191, 791–797.

    Article  CAS  Google Scholar 

  • Olberg, R. M., Seaman, R. C., Coats, M. I., & Henry, A. F. (2007). Eye movements and target fixation during dragonfly prey-interception flights. Journal of Comparative Physiology A, 193, 685–693.

    Article  CAS  Google Scholar 

  • Osorio, D., & Vorobyev, M. (2008). A review of the evolution of animal colour vision and visual communication signals. Vision Research, 48, 2042–2051.

    Article  PubMed  CAS  Google Scholar 

  • Paulson, D. R. (1966). The dragonflies (Odonata: Anisoptera) of southern Florida. Dissertation, University of Miami, Florida.

  • Peitsch, D., Feitz, A., Hertel, H., de Souza, J., Ventura, D. F., & Menzel, R. (1992). The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A, 170, 23–40.

    Article  CAS  Google Scholar 

  • Pritchard, G. (1966). On the morphology of the compound eyes of dragonflies (Odonata; Anisoptera). Proceedings of the Royal Entomological Society of London A, 43, 333–336.

    Google Scholar 

  • Rebora, M., & Piersanti, S. (2010). The antennal sensory function in the oldest pterygote insects: An ultrastructural overview. In D. J. Mendez-Vilas (Ed.), Microscopy: Science, technology, applications and education. Badajoz: Formatex Research Center.

    Google Scholar 

  • Roberts, N. W., Porter, M. L., & Cronin, T. W. (2011). The molecular basis of mechanisms underlying polarization vision. Philosophical Transactions of the Royal Society B, 366, 627–637.

    Article  CAS  Google Scholar 

  • Robertson, H. M. (1985). Female dimorphism and mating behaviour in a damselfly, Ischnura ramburii: Females mimicking males. Animal Behavior, 33, 805–809.

    Article  Google Scholar 

  • Schaller, F. (1960). Ètude du développement postembryonnaire d’Aeschna cyanea Müll. Annales des Sciences Naturelles-Zoologie et Biologie Animale, 2, 751–868.

    Google Scholar 

  • Schultz, T. D., Anderson, C. N., & Symes, L. B. (2008). The conspicuousness of colour cues in male pond damselflies depends on ambient light and visual system. Animal Behaviour, 76, 1357–1364.

    Article  Google Scholar 

  • Seki, T., Fujishita, S., & Obana, S. (1989). Composition and distribution of retinal and 3-hydroxyretinal in the compound eye of the dragonfly. Experimental Biology, 48, 65–75.

    PubMed  CAS  Google Scholar 

  • Shaw, K. L., & Mullen, S. P. (2011). Genes versus phenotypes in the study of speciation. Genetica, 139(5), 649–661.

    Article  PubMed  Google Scholar 

  • Sherk, T. E. (1978a). Development of the compound eyes of dragonflies (Odonata) II. Development of the larval compound eyes. Journal of Experimental Zoology, 203, 183–200.

    Article  PubMed  CAS  Google Scholar 

  • Sherk, T. E. (1978b). Development of the compound eyes of dragonflies (Odonata) III. Adult compound eyes. Journal of Experimental Zoology, 203, 61–80.

    Article  PubMed  CAS  Google Scholar 

  • Sherk, T. E. (1978c). Development of the compound eyes of dragonflies (Odonata) IV. Development of the adult compound eyes. Journal of Experimental Zoology, 203, 183–200.

    Article  PubMed  CAS  Google Scholar 

  • Sirot, L. K., Brockmann, H. J., Marinis, C., & Muschett, G. (2003). Maintenance of a female-limited polymorphism in Ischnura ramburi (Zygoptera:Coenagrionidae). Animal Behavior, 66, 763–775.

    Article  Google Scholar 

  • Snyder, A. W., Menzel, R., & Laughlin, S. B. (1973). Structure and function of the fused rhabdom. Journal of Comparative Physiology., 87, 99–135.

    Article  Google Scholar 

  • Stavenga, D. G. (2002). Colour in the eyes of insects. Journal of Comparative Physiology A- Neuroethology Sensory Neural and Behavioral Physiology, 188(5), 337–348.

    Article  CAS  Google Scholar 

  • Svensson, E. I., Abbott, J., & Härdling, R. (2005). Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations. American Naturalist, 165, 567–576.

    Article  PubMed  Google Scholar 

  • Svensson, E. I., Karlsson, K., Friberg, M., & Eroukhmanoff, F. (2007). Gender differences in species recognition and the evolution of asymmetric sexual isolation. Current Biology, 17, 1943–1947. doi:10.1016/j.cub.2007.09.038.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, Y., Yoshimura, J., Morita, S., & Watanabe, M. (2010). Negative frequency-dependent selection in female color polymorphism of a damselfly. Evolution, 64, 3620–3628. doi:10.1111/j.1558-5646.2010.01083.

    Article  PubMed  Google Scholar 

  • Tynkkynen, K., Rantala, M. J., & Suhonen, J. (2004). Interspecific aggression and character displacement in the damselfly Calopteryx splendens. Journal of Experimental Biology, 17, 759–767. doi:10.1111/j.1420-9101.2004.00733.x.

    CAS  Google Scholar 

  • Ueda, T. (1989). Sexual maturation, body colour changes and increase of body weight in a summer diapause population of the damselfly Lestes sponsa (Hansemann) (Zygoptera: Lestidae). Odonatologica, 18, 75–87.

    Google Scholar 

  • Van Gossum, H., Sherratt, T. N., & Cordero Rivera, A. (2008). The evolution of sex-limited colour polymorphism. In A. Córdoba-Aguilar (Ed.), Dragonflies: Model organisms for ecological and evolutionary research (pp. 219–229). Oxford: Oxford University Press.

    Google Scholar 

  • Van Gossum, H., Bots, J., Van Heusden, J., Hammers, M., Huyghe, K., & Morehouse, N. I. (2010). Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly Ischnura elegans. Evolutionary Ecology, 25, 139–154.

    Article  Google Scholar 

  • Waage, J. K. (1979). Dual function of the damselfly penis: Sperm removal and transfer. Science, 203, 916–918.

    Article  PubMed  CAS  Google Scholar 

  • Wakakuwa, M., Stavenga, D. G., & Arikawa, K. (2007). Spectral organization of ommatidia in flower-visiting insects. Phytochemical and Photobiology, 83, 27–34.

    Article  CAS  Google Scholar 

  • Warrant, E. J., & Nilsson, D.-E. (1995). The absorption of white light by photoreceptors. Vision Research, 38, 195–207.

    Article  Google Scholar 

  • Wehner, R. (1981). Spatial vision in arthropods. In H. Autrum (Ed.), Handbook of sensory physiology, Vol. VII/6C (pp. 287–616). Berlin: Springer.

    Google Scholar 

  • Williams, C. E. (1976). Neurocordulia (Platycordulia) xanthosoma (Williamson) in Texas (Odonata: Libellulidae: Corduliinae). Great Lakes Entomologist, 9, 63–73.

    Google Scholar 

  • Yamamoto, Y. (1968). A note on a gynandromorphic specimen of the dragonfly, Lyriothemis pachygastra Selys. New Entomologist, 17(2), 17–21.

    Google Scholar 

  • Yang, E.-C., & Osorio, D. (1991). Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly, Hemicordulia tau. Journal of Comparative Physiology A, 169, 663–669.

    Article  Google Scholar 

  • Yuan, F., Bernard, G. D., Le, J., & Briscoe, A. D. (2010). Contrasting modes of evolution of the visual pigments in Heliconius butterflies. Molecular Biology and Evolution, 27, 2392–2405.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are very grateful to the odonate community for their support of this work. We are particularly indebted to J. Abbott, S. Coleman and T. Davenport for providing images to support our figures that greatly improved the manuscript. We thank K. Tennessen and J. Ware for their encouragement and discussion along the way. We also thank M. May for his willingness to discuss and advance all aspects of odonate research, both the research presented herein and in our research broadly. We also thank E. Wilcox and the BYU DNA Sequencing Center for advice and the careful generation of the transcriptome data. This work was supported by the US National Science Foundation (MRI-0821728, IOS-1045243) and Brigham Young University.

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  1. Department of Biology, Brigham Young University, 401 WIDB, Provo, UT, 84602, USA

    Seth M. Bybee, K. Kaihileipihamekeola Johnson, Michael F. Whiting & Keith A. Crandall

  2. Integrative Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX, 78712, USA

    Eben J. Gering

  3. Monte L. Bean Life Science Museum, Brigham Young University, Provo, UT, 84602, USA

    Michael F. Whiting & Keith A. Crandall

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  1. Seth M. Bybee
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Correspondence to Seth M. Bybee.

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Seth M. Bybee and Kelsy K. Johnson contributed equally to this work.

This is a contribution to the Festschrift for Michael L. May

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Bybee, S.M., Johnson, K.K., Gering, E.J. et al. All the better to see you with: a review of odonate color vision with transcriptomic insight into the odonate eye. Org Divers Evol 12, 241–250 (2012). https://doi.org/10.1007/s13127-012-0090-6

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