1932

Abstract

Every aspect of vision, from the opsin proteins to the eyes and the ways that they serve animal behavior, is incredibly diverse. It is only with an evolutionary perspective that this diversity can be understood and fully appreciated. In this review, I describe and explain the diversity at each level and try to convey an understanding of how the origin of the first opsin some 800 million years ago could initiate the avalanche that produced the astonishing diversity of eyes and vision that we see today. Despite the diversity, many types of photoreceptors, eyes, and visual roles have evolved multiple times independently in different animals, revealing a pattern of eye evolution strictly guided by functional constraints and driven by the evolution of gradually more demanding behaviors. I conclude the review by introducing a novel distinction between active and passive vision that points to uncharted territories in vision research.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-121820-074736
2021-09-15
2024-10-11
Loading full text...

Full text loading...

/deliver/fulltext/vision/7/1/annurev-vision-121820-074736.html?itemId=/content/journals/10.1146/annurev-vision-121820-074736&mimeType=html&fmt=ahah

Literature Cited

  1. Agi E, Langen M, Altschuler SJ, Wu LF, Zimmermann T, Hiesinger PR. 2014. The evolution and development of neural superposition. J. Neurogenet. 28:216–32
    [Google Scholar]
  2. Allen AE, Martial FP, Lucas RJ. 2019. Form vision from melanopsin in humans. Nat. Commun. 10:2274
    [Google Scholar]
  3. Aranda ML, Schmidt TM. 2020. Diversity of intrinsically photosensitive retinal ganglion cells: circuits and functions. Cell. Mol. Life Sci 78:889–907
    [Google Scholar]
  4. Arendt D. 2017. The enigmatic xenopsins. eLife 6:e31781
    [Google Scholar]
  5. Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C et al. 2016. The origin and evolution of cell types. Nat. Rev. Genet. 17:744–57
    [Google Scholar]
  6. Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. 2004. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306:869–71
    [Google Scholar]
  7. Beckers P, von Döhren J 2016. Nemertea (Nemertini). Structure and Evolution of Invertebrate Nervous Systems A Schmidt-Rhaesa, S Harzsch, G Purschke 148–65 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  8. Berman D, Golomb JD, Walther DB. 2017. Scene content is predominantly conveyed by high spatial frequencies in scene-selective visual cortex. PLOS ONE 12:e0189828
    [Google Scholar]
  9. Blumer MJF. 1996. Alterations of the eyes during ontogenesis in Aporrhais pespelecani (Mollusca, Caenogastropoda). Zoomorphology 116:123–31
    [Google Scholar]
  10. Bok MJ, Capa M, Nilsson D-E. 2016. Here, there and everywhere: the radiolar eyes of fan worms (Annelida, Sabellidae). Integr. Comp. Biol. 56:784–95
    [Google Scholar]
  11. Bok MJ, Nilsson D-E. 2016. Fan worm eyes. Curr. Biol. 26:R1–3
    [Google Scholar]
  12. Bok MJ, Nilsson D-E, Garm A. 2019. Photoresponses in the radiolar eyes of the fan worm Acromegalomma vesiculosum. J. Exp. Biol. 222:jeb212779
    [Google Scholar]
  13. Bok MJ, Porter ML, Nilsson D-E. 2017a. Phototransduction in fan worm radiolar eyes. Curr. Biol. 27:R681–701
    [Google Scholar]
  14. Bok MJ, Porter ML, Ten Hove HA, Smith R, Nilsson D-E 2017b. Radiolar eyes of serpulid worms (Annelida, Serpulidae): structures, function, and phototransduction. Biol. Bull. 233:39–57
    [Google Scholar]
  15. Brady TF, Shafer-Skelton A, Alvarez GA. 2017. Global ensemble texture representations are critical to rapid scene perception. J. Exp. Psychol. Hum. Percept. Perform. 43:1160–76
    [Google Scholar]
  16. Buschbeck EK. 2005. The compound lens eye of Strepsiptera: morphological development of larvae and pupae. Arthropod Struct. Dev. 34:315–26
    [Google Scholar]
  17. Buschbeck EK. 2014. Escaping compound eye ancestry: the evolution of single-chamber eyes in holometabolous larvae. J. Exp. Biol. 217:2818–24
    [Google Scholar]
  18. Buschbeck EK, Ehmer B, Hoy RR. 2003. The unusual visual system of the Strepsiptera: external eye and neuropils. . J. Comp. Physiol. A 189:617–30
    [Google Scholar]
  19. Cronin TW, Johnsen S, Marshall NJ, Warrant EJ. 2014. Visual Ecology Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  20. Dodt E 1973. The parietal eye (pineal and parietal organs) of lower vertebrates. Handbook of Sensory Physiology: Central Processing of Visual Information Part B, ed. R Jung 113–40 Berlin: Springer
    [Google Scholar]
  21. Duelli P. 1978. An insect retina without microvilli in the male scale insect, Eriococcus sp. (Eriococcidae, Homoptera). Cell Tiss. Res. 187:417–27
    [Google Scholar]
  22. Eakin RM. 1965. Evolution of photoreceptors. Cold Spring Harbor Symp. Quant. Biol. 30:363–70
    [Google Scholar]
  23. Eaking RM, Brandenburger JL. 1981. Fine structure of the eyes of Pseudoceroscanadensis (Turbellaria, Polycladida). Zoomorphology 98:1–16
    [Google Scholar]
  24. Elofsson R. 2006. The frontal eyes of crustaceans. Arthropod Struct. Dev. 35:275–91
    [Google Scholar]
  25. Exner S. 1891. Die Physiologie du facettirten Augen von Krebsen und Insecten Leipzig, Ger: Deuticke
    [Google Scholar]
  26. Garm A, Andersson F, Nilsson D-E. 2008. Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. . Vis. Res. 48:1061–73
    [Google Scholar]
  27. Garm A, Bielecki J, Petie R, Nilsson D-E. 2016. Hunting in bioluminescent light: vision in the nocturnal box jellyfish Copula sivickisi. Front. Physiol. 7:99
    [Google Scholar]
  28. Garm A, Nilsson D-E. 2014. Visual navigation in starfish: first evidence for the use of vision and eyes in starfish. Proc. R. Soc. B 281:20133011
    [Google Scholar]
  29. Goodale MA, Milner AD. 1992. Separate visual pathways for perception and action. Trends Neurosci 15:20–25
    [Google Scholar]
  30. Goodale MA, Milner AD. 2018. Two visual pathways—where have they taken us and where will they lead in future?. Cortex 98:283–92
    [Google Scholar]
  31. Greene MR, Hansen BC. 2020. Disentangling the independent contributions of visual and conceptual features to the spatiotemporal dynamics of scene categorization. J. Neurosci. 40:5283–99
    [Google Scholar]
  32. Greene MR, Oliva A. 2009a. The briefest of glances: the time course of natural scene understanding. Psychol. Sci. 20:464–72
    [Google Scholar]
  33. Greene MR, Oliva A. 2009b. Recognition of natural scenes from global properties: seeing the forest without representing the trees. Cogn. Psychol. 58:137–76
    [Google Scholar]
  34. Gregory RL, HE Ross, Moray N. 1964. The curious eye of Copilia. Nature 201:1166–68
    [Google Scholar]
  35. Groen IIA, Silson EH, Baker CI. 2017. Contributions of low- and high-level properties to neural processing of visual scenes in the human brain. Phil. Trans. R. Soc. B 372:20160102
    [Google Scholar]
  36. Gühmann M, Jia H, Randel N, Verasztó C, Bezares-Calderón LA et al. 2015. Spectral tuning of phototaxis by a Go-opsin in the rhabdomeric eyes of Platynereis. Curr. Biol. 25:2265–71
    [Google Scholar]
  37. Harel A, Mzozoyana MW, Al Zoubi H, Nador JD, Noesen BT et al. 2020. Artificially-generated scenes demonstrate the importance of global scene properties for scene perception. Neuropsychologia 141:107434
    [Google Scholar]
  38. Heinze S. 2017. Unraveling the neural basis of insect navigation. Curr. Opin. Insect Sci. 24:58–67
    [Google Scholar]
  39. Hermans CO, Eakin RM 1974. Fine structure of the eyes of an alciopid polychaete, Vanadis tagensis (Annelida). Z. Morphol. Tiere 79:245–67
    [Google Scholar]
  40. Hughes HPI. 1976. Structure and regeneration of the eyes of strombid gastropods. Cell Tiss. Res. 171:259–71
    [Google Scholar]
  41. Hughes RL Jr., Woollacott RM. 1980. Photoreceptors of bryozoan larvae (Cheilostomata, Cellularioidea). Zool. Scr. 9:129–38
    [Google Scholar]
  42. Jékely G, Colombelli J, Hausen H, Guy K, Stelzer E et al. 2008. Mechanism of phototaxis in marine zooplankton. Nature 456:395–99
    [Google Scholar]
  43. Jonsen I. 2016. Joint estimation over multiple individuals improves behavioural state inference from animal movement data. Sci. Rep. 6:20625
    [Google Scholar]
  44. Jordana R, Baquero E, Montuenga LM. 2000. A new type of arthropod photoreceptor. Arthropod Struct. Dev. 29:289–93
    [Google Scholar]
  45. Kirschfeld K. 1967. Die Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge von Musca. Exp. Brain Res. 3:248–70
    [Google Scholar]
  46. Kirschfeld K 1976. The resolution of lens and compound eyes. Neural Principles in Vision F Zettler, R Weiler 354–70 Berlin: Springer
    [Google Scholar]
  47. Kirwan JD, Bok MJ, Smolka J, Foster JJ, Hernández JC, Nilsson D-E. 2018a. The sea urchin Diadema afrikanum uses low resolution vision to find shelter and deter enemies. J. Exp. Biol. 221:jeb176271
    [Google Scholar]
  48. Kirwan JD, Graf J, Smolka J, Mayer G, Henze MJ, Nilsson D-E. 2018b. Low resolution vision in a velvet worm (Onychophora). J. Exp. Biol. 221:jeb175802
    [Google Scholar]
  49. Knudsen EI. 2020. Evolution of neural processing for visual perception in vertebrates. J. Comp. Neurol. 528:2888–901
    [Google Scholar]
  50. Kohn JR, Heath SL, Behnia R. 2018. Eyes matched to the prize: the state of matched filters in insect visual circuits. Front. Neural Circuits 12:26
    [Google Scholar]
  51. Kojima D, Terakita A, Ishikawa T, Tsukahara Y, Maeda A, Shichida Y. 1997. A novel Go-mediated phototransduction cascade in scallop visual cells. . J. Biol. Chem. 272:22979–82
    [Google Scholar]
  52. Korsvig-Nielsen C, Hall M, Motti C, Garm A. 2019. Eyes and negative phototaxis in juvenile crown-of-thorns starfish, Acanthaster species complex. Biol. Open 8:bio041814
    [Google Scholar]
  53. Land MF 1984. Crustacea. Photoreception and Vision in Invertebrates MA Ali 401–38 New York: Plenum Press
    [Google Scholar]
  54. Land MF. 2019. Eyes to See: The Astonishing Variety of Vision in Nature Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  55. Land MF, Nilsson D-E. 2012. Animal Eyes Oxford, UK: Oxford Univ. Press, 2nd ed..
    [Google Scholar]
  56. Lehmann T, Heß M, Melzer RR. 2018. Sense organs in Pycnogonida: a review. Acta Zool 99:211–30
    [Google Scholar]
  57. Lucas RJ. 2013. Mammalian inner retinal photoreception. Curr. Biol. 23:R125–33
    [Google Scholar]
  58. Mahoney PJ, Young JK. 2017. Uncovering behavioural states from animal activity and site fidelity patterns. Methods Ecol. Evol. 8:174–83
    [Google Scholar]
  59. Maksimovic S, Layne JE, Buschbeck EK. 2007. Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera). J. Exp. Biol. 210:2819–28
    [Google Scholar]
  60. Malcolm GL, Groen IIA, Baker CI. 2016. Making sense of real-world scenes. Trends Cogn. Sci. 20:843–56
    [Google Scholar]
  61. Mandapaka K, Morgan RC, Buschbeck EK. 2006. Twenty-eight retinas but only twelve eyes: an anatomical analysis of the larval visual system of the diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae). J. Comp. Neurol. 497:166–81
    [Google Scholar]
  62. Mano H, Fukada Y. 2007. A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs. Photochem. Photobiol. 83:11–18
    [Google Scholar]
  63. Martín-Durán JM, Monjo F, Romero R. 2012. Morphological and molecular development of the eyes during embryogenesis of the freshwater planarian Schmidtea polychroa. Dev. Genes. Evol. 222:45–54
    [Google Scholar]
  64. Meyer-Rochow VB, Liddle AR 1988. Structure and function of the eyes of two species of opilionid from New Zealand glow-worm caves (Megalopsalis tiudam: Palpatores, and Hendea myersi cavernicola: Laniatores). Proc. R. Soc. Lond. B 233:293–319
    [Google Scholar]
  65. Mizunami M. 1994. Functional diversity of neural organization in insect ocellar systems. Vis. Res. 35:443–52
    [Google Scholar]
  66. Morehouse NI, Buschbeck EK, Zurek DB, Steck M, Porter ML. 2017. Molecular evolution of spider vision: new opportunities, familiar players. Biol. Bull. 233:21–38
    [Google Scholar]
  67. Morton B. 2008. The evolution of eyes in the Bivalvia: new insights. Am. Malacol. Bull. 26:35–45
    [Google Scholar]
  68. Mouland JW, Stinchcombe AR, Forger DB, Brown TM, Lucas RJ. 2017. Responses to spatial contrast in the mouse suprachiasmatic nuclei. Curr. Biol. 27:1633–40
    [Google Scholar]
  69. Muntz WRA, Raj U 1984. On the visual system of Nautilus pompilus. J. Exp. Biol. 109:253–63
    [Google Scholar]
  70. Nilsson D-E. 1983. Evolutionary links between apposition and superposition optics in crustacean eyes. Nature 302:818–21
    [Google Scholar]
  71. Nilsson D-E. 1988. A new type of imaging optics in compound eyes. Nature 332:76–78
    [Google Scholar]
  72. Nilsson D-E 1989. Optics and evolution of the compound eye. Facets of Vision DG Stavenga, R Hardie 30–73 Berlin: Springer
    [Google Scholar]
  73. Nilsson D-E. 1990a. From cornea to retinal image in invertebrate eyes. Trends Neurosci 13:55–64
    [Google Scholar]
  74. Nilsson D-E. 1990b. Three unexpected cases of refracting superposition eyes in crustaceans. J. Comp. Physiol. A 167:71–78
    [Google Scholar]
  75. Nilsson D-E. 1994. Eyes as optical alarm systems in fan worms and ark clams. Phil. Trans. R. Soc. B 346:195–212
    [Google Scholar]
  76. Nilsson D-E. 1996. Eye ancestry: old genes for new eyes. Curr. Biol. 6:39–42
    [Google Scholar]
  77. Nilsson D-E. 2009. The evolution of eyes and visually guided behaviour. Phil. Trans. R. Soc. B 364:2833–47
    [Google Scholar]
  78. Nilsson D-E. 2013. Eye evolution and its functional basis. Vis. Neurosci. 30:5–20
    [Google Scholar]
  79. Nilsson D-E. 2020. Eye evolution in animals. The Senses: A Comprehensive Reference, Vol. 1 B Fritzsch, PR Martin 96–121 Amsterdam: Elsevier, 2nd ed..
    [Google Scholar]
  80. Nilsson D-E, Bok MJ. 2017. Low-resolution vision—at the hub of eye evolution. Integr. Comp. Biol. 57:1066–70
    [Google Scholar]
  81. Nilsson D-E, Gislén L, Coates MM, Skogh C, Garm A. 2005. Advanced optics in a jellyfish eye. Nature 435:201–5
    [Google Scholar]
  82. Nilsson D-E, Kelber A. 2007. A functional analysis of compound eye evolution. Arthropod Struct. Dev. 36:373–85
    [Google Scholar]
  83. Nilsson D-E, Land MF, Howard J. 1984. Afocal apposition optics in butterfly eyes. Nature 312:561–63
    [Google Scholar]
  84. Nilsson D-E, Land MF, Howard J. 1988. Optics of the butterfly eye. J. Comp. Physiol. A 162:341–66
    [Google Scholar]
  85. Nilsson D-E, Marshall J 2020. Lens eyes in protists. Curr. Biol. 30:PR458–59
    [Google Scholar]
  86. Nilsson D-E, Ro A-I. 1994. Did neural pooling for night vision lead to the evolution of neural superposition eyes?. J. Comp. Physiol. A 175:289–302
    [Google Scholar]
  87. Nordström K, Wallén R, Seymour J, Nilsson D-E. 2003. A simple visual system without neurons in jellyfish larvae. Proc. R. Soc. Lond. B 270:2349–54
    [Google Scholar]
  88. O'Connor M, Garm A, Nilsson D-E. 2009. Structure and optics of the eyes of the box jellyfish Chiropsella bronzie. J. Comp. Physiol. A 195:557–69
    [Google Scholar]
  89. Osorio D. 2007. Spam and the evolution of the fly's eye. BioEssays 29:111–15
    [Google Scholar]
  90. Parker A. 2003. In the Blink of an Eye: How Vision Sparked the Big Bang of Evolution New York: Basic Books
    [Google Scholar]
  91. Paulus HF. 1979. Eye structure and the monophyly of the Arthropoda. In Arthropod Phylogeny AP Gupta 299–383 New York: Van Nostrand Reinhold
    [Google Scholar]
  92. Pergner J, Kozmik Z. 2017. Amphioxus photoreceptors—insights into the evolution of vertebrate opsins, vision and circadian rhythmicity. Int. J. Dev. Biol. 61:665–81
    [Google Scholar]
  93. Plachetzki DC, Oakley TH. 2007. Key transitions during the evolution of animal phototransduction: novelty, “tree-thinking,” co-option, and co-duplication. Integr. Comp. Biol. 47:759–69
    [Google Scholar]
  94. Purschke G, Arendt D, Hausen H, Müller MCM. 2006. Photoreceptor cells and eyes in Annelida. Arthropod Struct. Dev. 35:211–30
    [Google Scholar]
  95. Ramirez MD, Pairett AN, Pankey MS, Serb JM, Speiser DI et al. 2016. The last common ancestor of most bilaterian animals possessed at least nine opsins. Genome Biol. Evol. 8:3640–52
    [Google Scholar]
  96. Rawlinson KA, Lapraz F, Ballister ER, Terasaki M, Rodgers J et al. 2019. Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment. eLife 8:e45465
    [Google Scholar]
  97. Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM et al. 2012. Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J. Exp. Biol. 215:1278–86
    [Google Scholar]
  98. Ro A-I, Nilsson D-E. 1995. Pupil adjustments in the eye of the common backswimmer. J. Exp. Biol. 198:71–77
    [Google Scholar]
  99. Sapède D, Chaigne C, Blader P, Cau E. 2019. A novel subtype of pineal projection neurons expressing melanopsin share a common developmental program with classical projection neurons. bioRxiv 712091. http://dx.doi.org/10.1101/712091
    [Crossref]
  100. Seyer J-O. 1994. Structure and optics of the eye of the hawk-wing conch, Strombus raninus (L.). J. Exp. Zool. 268:200–7
    [Google Scholar]
  101. Seyer J-O, Nilsson DE, Warrant EJ. 1998. Spatial vision in the prosobranch gastropod Ampularia sp. J. Exp. Biol. 201:1673–79
    [Google Scholar]
  102. Speiser DI, Eernisse DJ, Johnsen S. 2011. A chiton uses aragonite lenses to form images. Curr. Biol. 21:665–70
    [Google Scholar]
  103. Stinchcombe AR, Mouland JW, Wong KY, Lucas RJ, Forger DB. 2017. Multiplexing visual signals in the suprachiasmatic nuclei. Cell Rep 21:1418–25
    [Google Scholar]
  104. Sumner-Rooney L, Kirwan JD, Lowe E, Ullrich-Lüter E. 2020. Extraocular vision in a brittle star is mediated by chromatophore movement in response to ambient light. Curr. Biol. 30:319–27
    [Google Scholar]
  105. Sumner-Rooney L, Rahman IA, Sigwart JD, Ullrich-Lüter E. 2018. Whole-body photoreceptor networks are independent of “lenses” in brittle stars. Proc. Biol. Sci. 285:20172590
    [Google Scholar]
  106. Suschenko D, Purschke G. 2008. Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution. Zoomorphology 128:75–96
    [Google Scholar]
  107. Terakita A, Kawano-Yamashita E, Koyanagi M. 2012. Evolution and diversity of opsins. WIREs Membr. Transp. Signal 1:104–11
    [Google Scholar]
  108. Van Hateren JH, Nilsson D-E. 1987. Butterfly optics exceed the theoretical limits of conventional apposition eyes. Biol. Cybern. 57:159–68
    [Google Scholar]
  109. Vernet G. 1979. Ultrastructure des photorecepteurs de Lineus ruber (O.F. Müller) (Hétéronémertes Lineidae). I. Ultrastructure de l'oeil normal. Z. Zellforsch. 104:494–50
    [Google Scholar]
  110. Vöcking O, Kourtesis I, Tumu SC, Hausen H 2017. Co-expression of xenopsin and rhabdomeric opsin in photoreceptors bearing microvilli and cilia. eLife 6:23435
    [Google Scholar]
  111. Vogt K. 1980. Die Spiegeloptik des Flußkrebsauge. . J. Comp. Physiol. 135:1–19
    [Google Scholar]
  112. 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]
  113. Vopalensky P, Pergner J, Liegertova M, Benito-Gutierrez E, Arendt D, Kozmik Z 2012. Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye. PNAS 109:15383–88
    [Google Scholar]
  114. Webb B, Wystrach A. 2016. Neural mechanisms of insect navigation. Curr. Opin. Insect Sci. 15:27–39
    [Google Scholar]
  115. Yerramilli D, Johnsen S. 2010. Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). J. Exp. Biol. 213:249–55
    [Google Scholar]
  116. Zeil J. 1979. A new kind of neural superposition eye: the compound eye of male Bibionidae. Nature 278:249–50
    [Google Scholar]
/content/journals/10.1146/annurev-vision-121820-074736
Loading
/content/journals/10.1146/annurev-vision-121820-074736
Loading

Data & Media loading...

  • 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