1932

Abstract

Color vision is widespread among insects but varies among species, depending on the spectral sensitivities and interplay of the participating photoreceptors. The spectral sensitivity of a photoreceptor is principally determined by the absorption spectrum of the expressed visual pigment, but it can be modified by various optical and electrophysiological factors. For example, screening and filtering pigments, rhabdom waveguide properties, retinal structure, and neural processing all influence the perceived color signal. We review the diversity in compound eye structure, visual pigments, photoreceptor physiology, and visual ecology of insects. Based on an overview of the current information about the spectral sensitivities of insect photoreceptors, covering 221 species in 13 insect orders, we discuss the evolution of color vision and highlight present knowledge gaps and promising future research directions in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-061720-071644
2021-01-07
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/en/66/1/annurev-ento-061720-071644.html?itemId=/content/journals/10.1146/annurev-ento-061720-071644&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    A'Brook J. 1973. Observations on different methods of aphid trapping. Ann. Appl. Biol. 74:263–77
    [Google Scholar]
  2. 2. 
    Akashi HD, Chen P-J, Akiyama T, Terai Y, Wakakuwa M et al. 2018. Physiological responses of ionotropic histamine receptors, PxHCLA and PxHCLB, to neurotransmitter candidates in a butterfly. Papilio xuthus. J. Exp. Biol. 221:jeb183129
    [Google Scholar]
  3. 3. 
    Aksoy V, Camlitepe Y. 2012. Behavioural analysis of chromatic and achromatic vision in the ant Formica cunicularia (Hymenoptera: Formicidae). Vis. Res. 67:28–36
    [Google Scholar]
  4. 4. 
    An L, Neimann A, Eberling E, Algora H, Brings S, Lunau K 2018. The yellow specialist: Dronefly Eristalis tenax prefers different yellow colours for landing and proboscis extension. J. Exp. Biol. 221:jeb184788
    [Google Scholar]
  5. 5. 
    Arikawa K. 2003. Spectral organization of the eye of a butterfly. Papilio. J. Comp. Physiol. A 189:791–800
    [Google Scholar]
  6. 6. 
    Arikawa K, Mizuno S, Kinoshita M, Stavenga DG 2003. Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of the butterfly Papilio xuthus. J. Neurosci 23:4527–32
    [Google Scholar]
  7. 7. 
    Arikawa K, Wakakuwa M, Qiu X, Kurasawa M, Stavenga DG 2005. Sexual dimorphism of short-wavelength photoreceptors in the small white butterfly. Pieris rapae crucivora. J. Neurosci. 25:5935–42
    [Google Scholar]
  8. 8. 
    Awata H, Wakakuwa M, Arikawa K 2009. Evolution of color vision in pierid butterflies: blue opsin duplication, ommatidial heterogeneity and eye regionalization in Colias erate. J. Comp. Physiol. A 195:401–8
    [Google Scholar]
  9. 9. 
    Balamurali GS, Edison A, Somanathan H, Kodandaramaiah U 2019. Spontaneous colour preferences and colour learning in the fruit-feeding butterfly. Mycalesis mineus. Behav. Ecol. Sociobiol. 73:39
    [Google Scholar]
  10. 10. 
    Behnia R, Desplan C. 2015. Visual circuits in flies: beginning to see the whole picture. Curr. Opin. Neurobiol. 34:125–32
    [Google Scholar]
  11. 11. 
    Bernard GD, Miller WH. 1968. Interference filters in the corneas of Diptera. Investig. Ophthalmol. Vis. Sci. 7:416–34
    [Google Scholar]
  12. 12. 
    Bernard GD, Remington CL. 1991. Color vision in Lycaena butterflies: spectral tuning of receptor arrays in relation to behavioral ecology. PNAS 88:2783–87
    [Google Scholar]
  13. 13. 
    Blake AJ, Pirih P, Qiu X, Arikawa K, Gries G 2019. Compound eyes of the small white butterfly Pieris rapae have three distinct classes of red photoreceptors. J. Comp. Physiol. A 205:553–65
    [Google Scholar]
  14. 14. 
    Booth D, Stewart AJA, Osorio D 2004. Colour vision in the glow-worm Lampyris noctiluca (L.) (Coleoptera: Lampyridae): evidence for a green-blue chromatic mechanism. J. Exp. Biol. 207:2373–78
    [Google Scholar]
  15. 15. 
    Brandt R, Vorobyev M. 1997. Metric analysis of threshold spectral sensitivity in the honeybee. Vis. Res. 37:425–39
    [Google Scholar]
  16. 16. 
    Brines ML, Gould JL. 1979. Bees have rules. Science 206:571–73
    [Google Scholar]
  17. 17. 
    Briscoe AD. 2008. Reconstructing the ancestral butterfly eye: Focus on the opsins. J. Exp. Biol. 211:1805–13
    [Google Scholar]
  18. 18. 
    Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annu. Rev. Entomol. 46:471–510
    [Google Scholar]
  19. 19. 
    Chen P-J, Awata H, Matsushita A, Yang E-C, Arikawa K 2016. Extreme spectral richness in the eye of the common bluebottle butterfly. Graphium sarpedon. Front. Ecol. Evol. 4:18
    [Google Scholar]
  20. 20. 
    Chen P-J, Belušič G, Arikawa K 2019. Chromatic information processing in the first optic ganglion of the butterfly Papilio xuthus. J. Comp. Physiol. A 206:199–216
    [Google Scholar]
  21. 21. 
    Chen P-J, Matsushita A, Wakakuwa M, Arikawa K 2019. Immunolocalization suggests a role of the histamine-gated chloride channel PxHCLB in spectral opponent processing in butterfly photoreceptors. J. Comp. Neurol. 527:753–66
    [Google Scholar]
  22. 22. 
    Cheng K, Collett TS, Wehner R 1986. Honeybees learn the colours of landmarks. J. Comp. Physiol. A 159:69–73
    [Google Scholar]
  23. 23. 
    Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded—why. Isr. J. Plant Sci. 45:115–27
    [Google Scholar]
  24. 24. 
    Chittka L, Menzel R. 1992. The evolutionary adaptation of flower colours and the insect pollinators’ colour vision. J. Comp. Physiol. A 171:171–81
    [Google Scholar]
  25. 25. 
    Collett TS. 1996. Insect navigation en route to the goal: multiple strategies for the use of landmarks. J. Exp. Biol. 199:227–35
    [Google Scholar]
  26. 26. 
    Crane J. 1955. Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Heiwitson, with special reference to the social use of color. Zoologica 40:167–96
    [Google Scholar]
  27. 27. 
    Cronin TW, Järvilehto M, Weckström M, Lall AB 2000. Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). J. Comp. Physiol. A 186:1–12
    [Google Scholar]
  28. 28. 
    Cronin TW, Porter ML. 2014. The evolution of invertebrate photopigments and photoreceptors. Evolution of Visual and Non-Visual Pigments DM Hunt, MW Hankins, SP Collin, NJ Marshall 105–35 Berlin: Springer
    [Google Scholar]
  29. 29. 
    Dacke M, Baird E, Warrant EJ, El Jundi B, Byrne M 2021. Celestial orientation and navigation in dung beetles. Annu. Rev. Entomol. 66: In press
    [Google Scholar]
  30. 30. 
    Daumer K. 1956. Reizmetrische Untersuchung des Farbensehens der Bienen. Z. Vgl. Physiol. 38:413–78
    [Google Scholar]
  31. 31. 
    Doering TF, Skellern M, Watts N, Cook SM 2012. Colour choice behaviour in the pollen beetle Meligethes aeneus (Coleoptera: Nitidulidae). Physiol. Entomol. 37:360–78
    [Google Scholar]
  32. 32. 
    Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MG, Simonov V, Wong BB 2012. Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc. R. Soc. B 279:3606–15
    [Google Scholar]
  33. 33. 
    Dyer AG, Boyd-Gerny S, Shrestha M, Garcia JE, van der Kooi CJ, Wong BBM 2019. Colour preferences of Tetragonula carbonaria stingless bees for colour morphs of the Australian native orchid Caladenia carnea. J. Comp. Physiol. A 205:347–61
    [Google Scholar]
  34. 34. 
    Eacock A, Rowland HM, van't Hof AE, Yung CJ, Edmonds N, Saccheri IJ 2019. Adaptive colour change and background choice behaviour in peppered moth caterpillars is mediated by extraocular photoreception. Commun. Biol. 2:286
    [Google Scholar]
  35. 35. 
    Edrich W, Neumeyer C, von Heiversen O 1979. “Anti-sun orientation” of bees with regard to a field of ultraviolet light. J. Comp. Physiol. 134:151–57
    [Google Scholar]
  36. 36. 
    El Jundi B, Pfeiffer K, Heinze S, Homberg U 2014. Integration of polarization and chromatic cues in the insect sky compass. J. Comp. Physiol. A 200:575–89
    [Google Scholar]
  37. 37. 
    El Jundi B, Warrant EJ, Byrne MJ, Khaldy L, Baird E et al. 2015. Neural coding underlying the cue preference for celestial orientation. PNAS 112:11395–400
    [Google Scholar]
  38. 38. 
    Finkbeiner SD, Fishman DA, Osorio D, Briscoe AD 2017. Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato. J. Exp. Biol 220:1267–76
    [Google Scholar]
  39. 39. 
    Fukushi T. 1990. Colour discrimination from various shades of grey in the trained blowfly. Lucilia cuprina. J. Insect Physiol. 36:69–75
    [Google Scholar]
  40. 40. 
    Futahashi R, Kawahara-Miki R, Kinoshita M, Yoshitake K, Yajima S et al. 2015. Extraordinary diversity of visual opsin genes in dragonflies. PNAS 112:E1247–56
    [Google Scholar]
  41. 41. 
    Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K 2000. In search of the visual pigment template. Vis. Neurosci. 17:509–28
    [Google Scholar]
  42. 42. 
    Goyret J, Markwell PM, Raguso RA 2007. The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J. Exp. Biol 210:1398–405
    [Google Scholar]
  43. 43. 
    Green CH. 1988. The effect of colour on trap- and screen-orientated responses in Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae). Bull. Entomol. Res. 78:591–604
    [Google Scholar]
  44. 44. 
    Green CH, Cosens D. 1983. Spectral responses of the tsetse fly. Glossina morsitans morsitans. J. Insect Physiol. 29:795–800
    [Google Scholar]
  45. 45. 
    Green CH, Flint S. 1986. An analysis of colour effects in the performance of the F2 trap against Glossina pallidipes Austen and G. morsitans morsitans Westwood (Diptera: Glossinidae). Bull. Entomol. Res. 76:409–18
    [Google Scholar]
  46. 46. 
    Hamdorf K, Hochstrate P, Höglund G, Moser M, Sperber S, Schlecht P 1992. Ultra-violet sensitizing pigment in blowfly photoreceptors R1–6; probable nature and binding sites. J. Comp. Physiol. A 171:601–15
    [Google Scholar]
  47. 47. 
    Hannah L, Dyer AG, Garcia JE, Dorin A, Burd M 2019. Psychophysics of the hoverfly: categorical or continuous color discrimination. Curr. Zool. 65:483–92
    [Google Scholar]
  48. 48. 
    Hardie J, Storer JR, Cook FJ, Campbell CAM, Wadhams LJ et al. 1996. Sex pheromone and visual trap interactions in mate location strategies and aggregation by host-alternating aphids in the field. Physiol. Entomol. 21:97–106
    [Google Scholar]
  49. 49. 
    Hardie RC. 1986. The photoreceptor array of the dipteran retina. Trends Neurosci 9:419–23
    [Google Scholar]
  50. 50. 
    Hardie RC. 1987. Is histamine a neurotransmitter in insect photoreceptors. J. Comp. Physiol. A 161:201–13
    [Google Scholar]
  51. 51. 
    Heath SL, Christenson MP, Oriol E, Saavedra-Weisenhaus M, Kohn JR, Behnia R 2020. Circuit mechanisms underlying chromatic encoding in Drosophila photoreceptors. Curr. Biol. 30:264–75.e8
    [Google Scholar]
  52. 52. 
    Hempel de Ibarra N, Vorobyev M, Menzel R 2014. Mechanisms, functions and ecology of colour vision in the honeybee. J. Comp. Physiol. A 200:411–33
    [Google Scholar]
  53. 53. 
    Henze MJ, Oakley TH. 2015. The dynamic evolutionary history of Pancrustacean eyes and opsins. Integr. Comp. Biol. 55:830–42
    [Google Scholar]
  54. 54. 
    Hiraga S. 2005. Two different sensory mechanisms for the control of pupal protective coloration in butterflies. J. Insect Physiol. 51:1033–40
    [Google Scholar]
  55. 55. 
    Ilić M, Pirih P, Belušič G 2016. Four photoreceptor classes in the open rhabdom eye of the red palm weevil, Rynchophorus ferrugineus Olivier. J. Comp. Physiol. A 202:203–13
    [Google Scholar]
  56. 56. 
    Ilse D. 1928. Über den Farbensinn der Tagfalter. Z. Vergl. Physiol. 8:658–92
    [Google Scholar]
  57. 57. 
    Ilse D. 1949. Colour discrimination in the dronefly. Eristalis tenax. Nature 163:255–56
    [Google Scholar]
  58. 58. 
    Jagadish S, Barnea G, Clandinin TR, Axel R 2014. Identifying functional connections of the inner photoreceptors in Drosophila using Tango-Trace. Neuron 83:630–44
    [Google Scholar]
  59. 59. 
    Kelber A. 1997. Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. J. Exp. Biol 200:827–36
    [Google Scholar]
  60. 60. 
    Kelber A. 1999. Ovipositing butterflies use a red receptor to see green. J. Exp. Biol. 202:2619–30
    [Google Scholar]
  61. 61. 
    Kelber A. 2001. Receptor based models for spontaneous colour choices in flies and butterflies. Entomol. Exp. Appl. 99:231–44
    [Google Scholar]
  62. 62. 
    Kelber A, Balkenius A, Warrant EJ 2002. Scotopic colour vision in nocturnal hawkmoths. Nature 419:922–25
    [Google Scholar]
  63. 63. 
    Kelber A, Henze MJ. 2013. Colour vision: parallel pathways intersect in Drosophila. Curr. Biol 23:R1043–45
    [Google Scholar]
  64. 64. 
    Kelber A, Osorio D. 2010. From spectral information to animal colour vision: experiments and concepts. Proc. R. Soc. B 277:1617–25
    [Google Scholar]
  65. 65. 
    Kelber A, Pfaff M. 1999. True colour vision in the orchard butterfly. Papilio aegeus. Naturwissenschaften 86:221–24
    [Google Scholar]
  66. 66. 
    Kelber A, Vorobyev M, Osorio D 2003. Animal colour vision—behavioural tests and physiological concepts. Biol. Rev. 78:81–118
    [Google Scholar]
  67. 67. 
    Kinoshita M, Pfeiffer K, Homberg U 2007. Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J. Exp. Biol 210:1350–61
    [Google Scholar]
  68. 68. 
    Kinoshita M, Shimada N, Arikawa K 1999. Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol 202:95–102
    [Google Scholar]
  69. 69. 
    Kinoshita M, Shimohigasshi M, Tominaga Y, Arikawa K, Homberg U 2015. Topographically distinct visual and olfactory inputs to the mushroom body in the Swallowtail butterfly. Papilio xuthus. J. Comp. Neurol. 523:162–82
    [Google Scholar]
  70. 70. 
    Kinoshita M, Stewart FJ, Ômura H 2017. Multisensory integration in Lepidoptera: insights into flower-visitor interactions. BioEssays 39:201600086
    [Google Scholar]
  71. 71. 
    Kirschfeld K, Franceschini N, Minke B 1977. Evidence for a sensitising pigment in fly photoreceptors. Nature 269:386–90
    [Google Scholar]
  72. 72. 
    Kirschfeld K, Hardie R, Lenz G, Vogt K 1988. The pigment system of the photoreceptor 7 yellow in the fly, a complex photoreceptor. J. Comp. Physiol. A 162:421–33
    [Google Scholar]
  73. 73. 
    Knoll F. 1921. Bombylius fuliginosus und die Farbe der Blumen. Insekten Blumen I. Abh. Zool.-Bot. Ges. Wien. 12:17–119
    [Google Scholar]
  74. 74. 
    Kong K-L, Fung YM, Wasserman GS 1980. Filter-mediated color vision with one visual pigment. Science 207:783–86
    [Google Scholar]
  75. 75. 
    Koshitaka H, Kinoshita M, Vorobyev M, Arikawa K 2008. Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc. R. Soc. B 275:947–54
    [Google Scholar]
  76. 76. 
    Kuenzinger W, Kelber A, Weesner J, Travis J, Raguso RA, Goyret J 2019. Innate colour preferences of a hawkmoth depend on visual context. Biol. Lett. 15:20180886
    [Google Scholar]
  77. 77. 
    Kugler H. 1950. Der Blütenbesuch der Schlammfliege (Eristalomyia tenax). Z. Vgl. Physiol. 32:328–47
    [Google Scholar]
  78. 78. 
    Kühn A. 1927. Über den Farbensinn der Bienen. Z. Vgl. Physiol. 5:762–800
    [Google Scholar]
  79. 79. 
    Land MF, Nilsson D-E. 2012. Animal Eyes Oxford, UK: Oxford Univ. Press
  80. 80. 
    Lebesa LN, Khan ZR, Hassanali A, Pickett JA, Bruce TJA et al. 2011. Responses of the blister beetle Hycleus apicicornis to visual stimuli. Physiol. Entomol. 36:220–29
    [Google Scholar]
  81. 81. 
    Lunau K, Knüttel H. 1995. Vision through colored eyes. Naturwissenschaften 82:432–34
    [Google Scholar]
  82. 82. 
    Lunau K, Maier EJ. 1995. Innate colour preferences of flower visitors. J. Comp. Physiol. A 177:1–19
    [Google Scholar]
  83. 83. 
    Lunau K, Wacht S. 1994. Optical releasers of the innate proboscis extension in the hoverfly Eristalis tenax L. (Syrphidae, Diptera). J. Comp. Physiol. A 174:575–79
    [Google Scholar]
  84. 84. 
    Mazzoni EO, Celik A, Wernet MF, Vasiliauskas D, Johnston RJ et al. 2008. Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLOS Biol 6:e97
    [Google Scholar]
  85. 85. 
    McCulloch KJ, Osorio D, Briscoe AD 2016. Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor. J. Exp. Biol. 219:2377–87
    [Google Scholar]
  86. 86. 
    McCulloch KJ, Yuan F, Zhen Y, Aardema ML, Smith G et al. 2017. Sexual dimorphism and retinal mosaic diversification following the evolution of a violet receptor in butterflies. Mol. Biol. Evol. 34:2271–84
    [Google Scholar]
  87. 87. 
    Meglič A, Ilić M, Pirih P, Škorjanc A, Wehling MF et al. 2019. Horsefly object-directed polarotaxis is mediated by a stochastically distributed ommatidial subtype in the ventral retina. PNAS 116:21843–53
    [Google Scholar]
  88. 88. 
    Melnattur KV, Pursley R, Lin T-Y, Ting C-Y, Smith PD et al. 2014. Multiple redundant medulla projection neurons mediate color vision in Drosophila. J. Neurogenet 28:374–88
    [Google Scholar]
  89. 89. 
    Menzel R. 1979. Spectral sensitivity and color vision in invertebrates. Handbook of Sensory Physiology, Vol. VII/6A, ed. H Autrum 503–80 Berlin: Springer
    [Google Scholar]
  90. 90. 
    Menzel R, Blakers M. 1976. Colour receptors in the bee eye—morphology and spectral sensitivity. J. Comp. Physiol. A 108:11–13
    [Google Scholar]
  91. 91. 
    Menzel R, Ventura DF, Werner A, Joaquim LCM, Backhaus W 1989. Spectral sensitivity of single photoreceptors and color vision in the stingless bee. Melipona quadrifasciata. J. Comp. Physiol. A 166:151–64
    [Google Scholar]
  92. 92. 
    Moericke V. 1949. Über den Farbensinn der Pfirsichblattlaus (Myzodes persicae Sulz.). Anz. Schädlingskd. 22:139
    [Google Scholar]
  93. 93. 
    Möller R. 2002. Insects could exploit UV-green contrast for landmark navigation. J. Theor. Biol. 214:619–31
    [Google Scholar]
  94. 94. 
    Morehouse NI, Rutowski RL. 2010. In the eyes of the beholders: female choice and avian predation risk associated with an exaggerated male butterfly color. Am. Nat. 176:768–84
    [Google Scholar]
  95. 95. 
    Ogawa Y, Kinoshita M, Stavenga DG, Arikawa K 2013. Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the eastern pale clouded yellow butterfly. Colias erate. J. Exp. Biol. 216:1916–23
    [Google Scholar]
  96. 96. 
    Oonincx D, Volk N, Diehl JJE, Van Loon JJA, Belušič G 2016. Photoreceptor spectral sensitivity of the compound eyes of black soldier fly (Hermetia illucens) informing the design of LED-based illumination to enhance indoor reproduction. J. Insect Physiol. 95:133–39
    [Google Scholar]
  97. 97. 
    O'Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, Applebury ML 1985. The Drosophila ninaE gene encodes an opsin. Cell 40:839–50
    [Google Scholar]
  98. 98. 
    Paulk AC, Dacks AM, Phillips-Portillo J, Fellous J-M, Gronenberg W 2009. Visual processing in the central bee brain. J. Neurosci. 29:9987–99
    [Google Scholar]
  99. 99. 
    Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R 1992. The spectral input systems of hymenopteran insects and their receptor-based color vision. J. Comp. Physiol. A 170:23–40
    [Google Scholar]
  100. 100. 
    Perry M, Kinoshita M, Saldi G, Huo L, Arikawa K, Desplan C 2016. Molecular logic behind the three-way stochastic choices that expand butterfly colour vision. Nature 535:280–84
    [Google Scholar]
  101. 101. 
    Prokopy RJ, Economopoulos AP, McFadden MW 1975. Attraction of wild and laboratory-cultured Dacus oleae flies to small rectangles of different hues, shades, and tints. Entomol. Exp. Appl. 18:141–52
    [Google Scholar]
  102. 102. 
    Prokopy RJ, Owens ED. 1983. Visual detection of plants by herbivorous insects. Annu. Rev. Entomol. 28:337–64
    [Google Scholar]
  103. 103. 
    Qiu X, Vanhoutte KAJ, Stavenga DG, Arikawa K 2002. Ommatidial heterogeneity in the compound eye of the male small white butterfly. Pieris rapae crucivora. Cell Tissue Res. 307:371–79
    [Google Scholar]
  104. 104. 
    Scherer C, Kolb G. 1987. The influence of color stimuli on visually controlled behavior in Aglais urticae L. and Pararge aegeria L. (Lepidoptera). J. Comp. Physiol. A 161:891–98
    [Google Scholar]
  105. 105. 
    Schmeling F, Wakakuwa M, Tegtmeier J, Kinoshita M, Bockhorst T et al. 2014. Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust. Schistocerca gregaria. J. Exp. Biol. 217:3557–68
    [Google Scholar]
  106. 106. 
    Schnaitmann C, Garbers C, Wachtler T, Tanimoto H 2013. Color discrimination with broadband photoreceptors. Curr. Biol. 23:2375–82
    [Google Scholar]
  107. 107. 
    Schnaitmann C, Haikala V, Abraham E, Oberhauser V, Thestrup T et al. 2018. Color processing in the early visual system of Drosophila. Cell 172:318–30
    [Google Scholar]
  108. 108. 
    Schremmer F. 1941. Sinnesphysiologie und Blumenbesuch des Falters von Plusia gamma L. Zool. Jahrb. Abt. Syst. Ökol. 74:375–435
    [Google Scholar]
  109. 109. 
    Schremmer F. 1941. Versuche zum Nachweis der Rotblindheit von Vespa rufa L. Z. Vgl. Physiol. 28:457–66
    [Google Scholar]
  110. 110. 
    Schröder R, Linkem CN, Rivera JA, Butler MA 2018. Should I stay or should I go? Perching damselfly use simple colour and size cues to trigger flight. Anim. Behav. 145:29–37
    [Google Scholar]
  111. 111. 
    Shafir S. 1996. Color discrimination conditioning of a wasp, Polybia occidentalis (Hymenoptera: Vespidae). Biotropica 28:243–51
    [Google Scholar]
  112. 112. 
    Sharkey CR, Fujimoto MS, Lord NP, Shin S, McKenna DD et al. 2017. Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles. Sci. Rep. 7:8
    [Google Scholar]
  113. 113. 
    Shaw SR. 1975. Retinal resistance barriers and electrical lateral inhibition. Nature 255:480–83
    [Google Scholar]
  114. 114. 
    Shrestha M, Burd M, Garcia JE, Dorin A, Dyer AG 2019. Colour evolution within orchids depends on whether the pollinator is a bee or a fly. Plant Biol 21:745–52
    [Google Scholar]
  115. 115. 
    Sison-Mangus MP, Briscoe AD, Zaccardi G, Knüttel H, Kelber A 2008. The lycaenid butterfly Polyommatus icarus uses a duplicated blue opsin to see green. J. Exp. Biol. 211:361–69
    [Google Scholar]
  116. 116. 
    Snyder AW, Menzel R, Laughlin SB 1973. Structure and function of the fused rhabdom. J. Comp. Physiol. A 87:99–135
    [Google Scholar]
  117. 117. 
    Somanathan H, Borges RM, Warrant EJ, Kelber A 2008. Nocturnal bees learn landmark colours in starlight. Curr. Biol. 18:R996–97
    [Google Scholar]
  118. 118. 
    Spaethe J, Briscoe AD. 2005. Molecular characterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina. J. Exp. Biol. 208:2347–61
    [Google Scholar]
  119. 119. 
    Spaethe J, Streinzer M, Eckert J, May S, Dyer AG 2014. Behavioural evidence of colour vision in free flying stingless bees. J. Comp. Physiol. A 200:485–96
    [Google Scholar]
  120. 120. 
    Stavenga DG. 2002. Colour in the eyes of insects. J. Comp. Physiol. A 188:337–48
    [Google Scholar]
  121. 121. 
    Stavenga DG. 2003. Angular and spectral sensitivity of fly photoreceptors. I. Integrated facet lens and rhabdomere optics. J. Comp. Physiol. A 189:1–17
    [Google Scholar]
  122. 122. 
    Stavenga DG, Smits RP, Hoenders BJ 1993. Simple exponential functions describing the absorbance bands of visual pigment spectra. Vis. Res. 33:1011–17
    [Google Scholar]
  123. 123. 
    Stewart FJ, Kinoshita M, Arikawa K 2015. The butterfly Papilio xuthus detects visual motion using chromatic contrast. Biol. Lett. 11:20150687
    [Google Scholar]
  124. 124. 
    Stöckl A, Heinze S, Charalabidis A, El Jundi B, Warrant E, Kelber A 2016. Differential investment in visual and olfactory brain areas reflects behavioural choices in hawk moths. Sci. Rep. 6:26041
    [Google Scholar]
  125. 125. 
    Streinzer M, Roth N, Paulus HF, Spaethe J 2019. Color preference and spatial distribution of glaphyrid beetles suggest a key role in the maintenance of the color polymorphism in the peacock anemone (Anemone pavonina, Ranunculaceae) in Northern Greece. J. Comp. Physiol. A 205:735–43
    [Google Scholar]
  126. 126. 
    Süffert F, Götz B. 1936. Verhalten von Schmetterlingsraupen gegenüber farbigen Flächen. Naturwissenschaften 24:815
    [Google Scholar]
  127. 127. 
    Sugihara T, Nagata T, Mason B, Koyanagi M, Terakita A 2016. Absorption characteristics of vertebrate non-visual opsin, Opn3. PLOS ONE 11:e0161215
    [Google Scholar]
  128. 128. 
    Swihart CA, Swihart SL. 1970. Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn. Anim. Behav. 18:60–64
    [Google Scholar]
  129. 129. 
    Takemura S, Arikawa K. 2006. Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly. Papilio xuthus. J. Comp. Neurol. 494:663–72
    [Google Scholar]
  130. 130. 
    Takemura S, Xu CS, Lu Z, Rivlin PK, Parag T et al. 2015. Synaptic circuits and their variations within different columns in the visual system of Drosophila. PNAS 112:13711–16
    [Google Scholar]
  131. 131. 
    Takeuchi Y, Arikawa K, Kinoshita M 2006. Color discrimination at the spatial resolution limit in a swallowtail butterfly. Papilio xuthus. J. Exp. Biol. 209:2873–79
    [Google Scholar]
  132. 132. 
    Telles FJ, Kelber A, Rodríguez-Gironés MA 2016. Wavelength discrimination in the hummingbird hawkmoth Macroglossum stellatarum. J. Exp. Biol 219:553–60
    [Google Scholar]
  133. 133. 
    Telles FJ, Lind O, Henze MJ, Rodríguez-Gironés MA, Goyret J, Kelber A 2014. Out of the blue: the spectral sensitivity of hummingbird hawkmoths. J. Comp. Physiol. A 200:537–46
    [Google Scholar]
  134. 134. 
    Troje N. 1993. Spectral categories in the learning behaviour of blowflies. Z. Naturforsch. C 48:96–104
    [Google Scholar]
  135. 135. 
    van der Kooi CJ, Dyer AG, Kevan PG, Lunau K 2019. Functional significance of the optical properties of flowers for visual signalling. Ann. Bot. 123:263–76
    [Google Scholar]
  136. 136. 
    van der Kooi CJ, Elzenga JTM, Staal M, Stavenga DG 2016. How to colour a flower: on the optical principles of flower coloration. Proc. R. Soc. B 283:20160429
    [Google Scholar]
  137. 137. 
    van der Kooi CJ, Ollerton J 2020. The origins of flowering plants and animal pollination. Science 368:1306–8
    [Google Scholar]
  138. 138. 
    Vasas V, Peng F, MaBouDi H, Chittka L 2019. Randomly weighted receptor inputs can explain the large diversity of colour-coding neurons in the bee visual system. Sci. Rep. 9:8330
    [Google Scholar]
  139. 139. 
    Vogt K, Aso Y, Hige T, Knapek S, Ichinose T et al. 2016. Direct neural pathways convey distinct visual information to Drosophila mushroom bodies. eLife 5:e14009
    [Google Scholar]
  140. 140. 
    von Beier W, Menzel R 1972. Untersuchungen über den Farbensinn der deutschen Wespe (Paravespula germanica F., Hymenoptera, Vespidae): Verhaltensphysiologischer nachweis des Farbensehens. Zool. Jahrb. Physiol. 76:441–54
    [Google Scholar]
  141. 141. 
    Von Frisch K. 1914. Der Farbensinn und Formensinn der Biene. Zool. Jahrb. Abt. Allg. Zool. Physiol. Tiere 35:1–188
    [Google Scholar]
  142. 142. 
    Von Helversen O. 1972. Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J. Comp. Physiol. A 80:439–72
    [Google Scholar]
  143. 143. 
    Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K 2005. Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92:464–67
    [Google Scholar]
  144. 144. 
    Wakakuwa M, Stavenga DG, Arikawa K 2007. Spectral organization of ommatidia in flower-visiting insects. Photochem. Photobiol. 83:27–34
    [Google Scholar]
  145. 145. 
    Wakakuwa M, Stavenga DG, Kurasawa M, Arikawa K 2004. A unique visual pigment expressed in green, red and deep-red receptors in the eye of the small white butterfly. Pieris rapae crucivora. J. Exp. Biol. 207:2803–10
    [Google Scholar]
  146. 146. 
    Warrant EJ, Nilsson D-E. 1998. Absorption of white light in photoreceptors. Vis. Res. 38:195–207
    [Google Scholar]
  147. 147. 
    Wehner R. 1987. “Matched filters”—neural models of the external world. J. Comp. Physiol. A 161:511–31
    [Google Scholar]
  148. 148. 
    Wernet MF, Perry MW, Desplan C 2015. The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic. Trends Genet 31:316–28
    [Google Scholar]
  149. 149. 
    Yilmaz A, Dyer AG, Rössler W, Spaethe J 2017. Innate colour preference, individual learning and memory retention in the ant Camponotus blandus. J. Exp. Biol 220:3315–26
    [Google Scholar]
  150. 150. 
    Zaccardi G, Kelber A, Sison-Mangus MP, Briscoe AD 2006. Color discrimination in the red range with only one long-wavelength sensitive opsin. J. Exp. Biol. 209:1944–55
    [Google Scholar]
/content/journals/10.1146/annurev-ento-061720-071644
Loading
/content/journals/10.1146/annurev-ento-061720-071644
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error