Genetic Regulation of Early Eye Development in Non-dipteran Insects

  • Markus FriedrichEmail author
  • Ying Dong
  • Zhenyi Liu
  • Iris Yang


Comparative analyses of eye development in Drosophila and distantly related phyla have fundamentally changed the way we think about the evolution of animal eyes today. On the one hand, it is clear that select eye-patterning mechanisms have deep evolutionary roots, such as the involvement of Pax6 and an ever-extending catalogue of additional transcription factors with selector gene-like functions in development. On the other hand, the diversity of distinct eye types in extant animals implies the evolution of lineage-specific patterning processes, superimposed onto the ancient gene interactions inherited from the prototype eye at the dawn of animal evolution. Therefore, an important question to consider is how far back the regulatory program organizing the development of the compound eye in Drosophila can be traced to arthropod evolution.


Holometabolous Insect Retinal Differentiation Morphogenetic Furrow Antennal Disc Antennal Imaginal Disc 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to Amit Singh for the invitation to provide this book chapter, Rewaa Yas for meticulous proofreading of the manuscript,and Dr. Sumihare Noji for providing Fig. 7. Research in the Friedrich lab has been supported by NSF awards IOS 0951886, IOS 0091926, and EF-0334948.


  1. Allee JP, Pelletier CL, Fergusson EK, Champlin DT (2006) Early events in adult eye development of the moth, Manduca sexta. J Insect Physiol 52:450–460PubMedCrossRefGoogle Scholar
  2. Anderson H (1978) Postembryonic development of the visual system of the locust, Schistocerca gregaria. I. Pattern of growth and developmental interactions in the retina and optic lobe. J Embryol Exp Morphol 45:55–83PubMedGoogle Scholar
  3. Baker NE (2001) Master regulatory genes; telling them what to do. Bioessays 23:763–766PubMedCrossRefGoogle Scholar
  4. Baonza A, Freeman M (2002) Control of Drosophila eye specification by Wingless signalling. Development 129:5313–5322PubMedCrossRefGoogle Scholar
  5. Bennet RR, Tunstall J, Horridge GA (1967) Spectral sensitivity of single retinula cells in the locust. Z Vgl Physiol 55:195–206CrossRefGoogle Scholar
  6. Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47–74PubMedGoogle Scholar
  7. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS (2002) Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev 16:2415–2427PubMedCrossRefGoogle Scholar
  8. Beutel RG, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F, Beckmann F, Meier R, Misof B, Whiting MF, Vilhelmsen L (2011) Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27:341–355CrossRefGoogle Scholar
  9. Blackburn DC, Conley KW, Plachetzki DC, Kempler K, Battelle BA, Brown NL (2008) Isolation and expression of Pax6 and atonal homologues in the American horseshoe crab, Limulus polyphemus. Dev Dyn 237:2209–2219PubMedCrossRefGoogle Scholar
  10. Blum M, Labhart T (2000) Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 186:119–128CrossRefGoogle Scholar
  11. Bodenstein D (1953) Postembryonic development. In: Roeder KD (ed) Insect Physiology. Wiley, New York, pp 275–367Google Scholar
  12. Brown SJ, Shippy TD, Miller S, Bolognesi R, Beeman RW, Lorenzen MD, Bucher G, Wimmer EA, Klingler M (2009) The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology. Cold Spring Harb Protoc pdb.emo126Google Scholar
  13. Buschbeck E, Friedrich M (2008) Evolution of insect eyes: tales of ancient heritage, deconstruction, reconstruction, remodeling and recycling. Evolution Education and Outreach 1:448–462CrossRefGoogle Scholar
  14. Buschbeck EK (2005) The compound lens eye of Strepsiptera: morphological development of larvae and pupae. Arthropod Struct Dev 34:315–326CrossRefGoogle Scholar
  15. Buschbeck EK, Roosevelt JL, Hoy RR (2001) Eye stalks or no eye stalks: a structural comparison of pupal development in the stalk-eyed fly Cyrtodiopsis and in Drosophila. J Comp Neurol 433:486–498PubMedCrossRefGoogle Scholar
  16. Cavodeassi F, Diez Del Corral R, Campuzano S, Dominguez M (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126:4933–4942PubMedGoogle Scholar
  17. Cavodeassi F, Modolell J, Campuzano S (2000) The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development 127:1921–1929PubMedGoogle Scholar
  18. Champlin DT, Truman JW (1998) Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta. Development 125:2009–2018PubMedGoogle Scholar
  19. Chang T, Mazotta J, Dumstrei K, Dumitrescu A, Hartenstein V (2001) Dpp and Hh signaling in the Drosophila embryonic eye field. Development 128:4691–4704PubMedGoogle Scholar
  20. Cho KO, Choi KW (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396:272–276PubMedCrossRefGoogle Scholar
  21. Dearden P, Akam M (2000) A role for Fringe in segment morphogenesis but not segment formation in the grasshopper, Schistocerca gregaria. Development Genes Evolution 210:329–336PubMedCrossRefGoogle Scholar
  22. Dominguez M, Casares F (2005) Organ specification-growth control connection: new in-sights from the Drosophila eye-antennal disc. Dev Dyn 232:673–684PubMedCrossRefGoogle Scholar
  23. Dominguez M, de Celis JF (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396:276–278PubMedCrossRefGoogle Scholar
  24. Dominguez M, Ferres-Marco D, Gutierrez-Avino FJ, Speicher SA, Beneyto M (2004) Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster. Nat Genet 36:31–39PubMedCrossRefGoogle Scholar
  25. Dong Y, Friedrich M (2005) Comparative analysis of Wg patterning in the embryonic grasshopper eye. Dev Genes Evol 215:177–197PubMedCrossRefGoogle Scholar
  26. Dong Y, Friedrich M (2010) Enforcing biphasic eye development in a directly developing insect by transient knockdown of single eye selector genes. J Exp Zool B Mol Dev Evol 314B:104–114Google Scholar
  27. Dong Y, Dinan L, Friedrich M (2003) The effect of manipulating ecdysteroid signaling on embryonic eye development in the locust Schistocerca americana. Dev Genes Evol 213:587–600PubMedCrossRefGoogle Scholar
  28. Donner AL, Maas RL (2004) Conservation and non-conservation of genetic pathways in eye specification. Int J Dev Biol 48:743–753PubMedCrossRefGoogle Scholar
  29. Duman-Scheel M, Pirkl N, Patel NH (2002) Analysis of the expression pattern of Mysidium columbiae wingless provides evidence for conserved mesodermal and retinal patterning processes among insects and crustaceans. Dev Genes Evol 212:114–123PubMedCrossRefGoogle Scholar
  30. Egelhaaf A (1988) Evidence for the priming role of the central retinula cell in ommatidium differentiation of Ephestia kuehniella. Rouxs Arch Dev Biol 197:184–189CrossRefGoogle Scholar
  31. Erezyilmaz DF, Riddiford LM, Truman JW (2006) The pupal specifier broad directs progressive morphogenesis in a direct-developing insect. Proc Natl Acad Sci 103:6925–6930PubMedCrossRefGoogle Scholar
  32. Fahrenbach WH (1969) The morphology of the eyes of Limulus. II. Ommatidia of the compound eye. Z Zellforsch Mikrosk Anat 93:451–483PubMedCrossRefGoogle Scholar
  33. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  34. Friedrich M (2006) Continuity versus split and reconstitution: exploring the molecular developmental corollaries of insect eye primordium evolution. Dev Biol 299:310–329PubMedCrossRefGoogle Scholar
  35. Friedrich M (2008) Opsins and cell fate in the Drosophila Bolwig organ: tricky lessons in homology inference. Bioessays 30:980–993PubMedCrossRefGoogle Scholar
  36. Friedrich M, Benzer S (2000) Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis. J Exp Zool B Mol Dev E 288:39–55CrossRefGoogle Scholar
  37. Friedrich M, Caravas J (2011) New insights from hemichordate genomes: prebilaterian origin and parallel modifications in the paired domain of the Pax gene eyegone. J Exp Zool B Mol Dev E 316:387–392CrossRefGoogle Scholar
  38. Friedrich M, Rambold I, Melzer RR (1996) The early stages of ommatidial development in the flour beetle Tribolium castaneum (Coleoptera, Tenebrionidae). Dev Genes Evol 206:136–146CrossRefGoogle Scholar
  39. Friedrich M, Dong Y, Jackowska M (2006) Insect interordinal relationships: insights from the visual system. Arthropod Syst Phylogeny 64:133–148Google Scholar
  40. Gehring WJ (2002) The genetic control of eye development and its implications for the evolution of the various eye-types. Int. J. Dev Biol 46:65–73PubMedGoogle Scholar
  41. Greenwood S, Struhl G (1999) Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development 126:5795–5808PubMedGoogle Scholar
  42. Hafner GS, Tokarski TR (1998) Morphogenesis and pattern formation in the retina of the crayfish Procambarus clarkii. Cell Tissue Res 293:535–550PubMedCrossRefGoogle Scholar
  43. Hafner GS, Tokarski TR (2001) Retinal development in the lobster Homarus americanus. Comparison with compound eyes of insects and other crustaceans. Cell Tissue Res 305:147–158PubMedCrossRefGoogle Scholar
  44. Harzsch S, Walossek D (2001) Neurogenesis in the developing visual system of the branchiopod crustacean Triops longicaudatus (LeConte, 1846): corresponding patterns of compound-eye formation in Crustacea and Insecta? Dev Genes Evol 211:37–43PubMedCrossRefGoogle Scholar
  45. Heberlein U, Wolff T, Rubin GM (1993) The TGF beta homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75:913–926PubMedCrossRefGoogle Scholar
  46. Henze MJ, Dannenhauer K, Kohler M, Labhart T, Gesemann M (2012) Opsin evolution and expression in arthropod compound eyes and ocelli: Insights from the cricket Gryllus bimaculatus. BMC Evol Biol 12:163PubMedCrossRefGoogle Scholar
  47. Homberg U, Paech A (2002) Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30:271–280PubMedCrossRefGoogle Scholar
  48. Inoue Y, Miyawaki K, Terasawa T, Matsushima K, Shinmyo Y, Niwa N, Mito T, Ohuchi H, Noji S (2004) Expression patterns of dachshund during head development of Gryllus bimaculatus (cricket). Gene Expr Patterns 4:725–731PubMedCrossRefGoogle Scholar
  49. Jackowska M, Bao R, Liu Z, McDonald EC, Cook TA, Friedrich M (2007) 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. Front Zool 4:24PubMedCrossRefGoogle Scholar
  50. Jun S, Wallen RV, Goriely A, Kalionis B, Desplan C (1998) Lune/eye gone, a Pax-like protein, uses a partial paired domain and a homeodomain for DNA recognition. Proc Natl Acad Sci U S A 95:13720–13725PubMedCrossRefGoogle Scholar
  51. Kenyon KL, Ranade SS, Curtiss J, Mlodzik M, Pignoni F (2003) Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Dev Cell 5:403–414PubMedCrossRefGoogle Scholar
  52. Klingler M (2004) Tribolium. Curr Biol 14:R639–R640PubMedCrossRefGoogle Scholar
  53. Konopova B, Jindra M (2008) Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development 135:559–568PubMedCrossRefGoogle Scholar
  54. Koyama T, Syropyatova MO, Riddiford LM (2008) Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone. Dev Biol 324:258–265PubMedCrossRefGoogle Scholar
  55. Kozmik Z (2008) The role of Pax genes in eye evolution. Brain Res Bull 75:335–339PubMedCrossRefGoogle Scholar
  56. Kristensen N (1999) Phylogeny of edopterygote insects, the most successful lineage of living organisms. Eur J Entomol 96:237–253Google Scholar
  57. Kronhamn J, Frei E, Daube M, Jiao R, Shi Y, Noll M, Rasmuson-Lestander A (2002) Headless flies produced by mutations in the paralogous Pax6 genes eyeless and twin of eyeless. Development 129:1015–1026PubMedGoogle Scholar
  58. Kumar JP (2009) The molecular circuitry governing retinal determination. Biochim Biophys Acta 1789:306–314PubMedCrossRefGoogle Scholar
  59. Kumar JP, Moses K (2001) The EGF receptor and Notch signaling pathways control the initiation of the morphogenetic furrow during Drosophila eye development. Development 128:2689–2697PubMedGoogle Scholar
  60. Labhart T, Keller K (1992) Fine structure and growth of the polarization-sensitive dorsal rim area in the compound eye of larval crickets. Naturwissenschaften 79:527–529CrossRefGoogle Scholar
  61. Labhart T, Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47:368–379PubMedCrossRefGoogle Scholar
  62. Lamb T (2011) Evolution’s witness: how eyes evolved. Oxford University Press, USAGoogle Scholar
  63. Lee JD, Treisman JE (2001) The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc. Development 128:1519–1529PubMedGoogle Scholar
  64. Lee MSY, Jago JB, Garcia-Bellido DC, Edgecombe GD, Gehling JG, Paterson JR (2011) Modern optics in exceptionally preserved eyes of Early Cambrian arthropods from Australia. Nature 474:631–634PubMedCrossRefGoogle Scholar
  65. Liu Z, Friedrich M (2004) The Tribolium homologue of glass and the evolution of insect larval eyes. Dev Biol 269:36–54PubMedCrossRefGoogle Scholar
  66. Liu Z, Yang X, Dong Y, Friedrich M (2006) Tracking down the “head blob”: comparative analysis of wingless expression in the embryonic insect procephalon reveals progressive reduction of ocular segment patterning in higher insects. Arthropod Struct Dev 35:341–356PubMedCrossRefGoogle Scholar
  67. Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702PubMedCrossRefGoogle Scholar
  68. Lorenz MW (2007) Oogenesis-flight syndrome in crickets: age-dependent egg production, flight performance, and biochemical composition of the flight muscles in adult female Gryllus bimaculatus. J Insect Physiol 53:819–832PubMedCrossRefGoogle Scholar
  69. Lynch V, Wagner G (2011) Revisiting a classic example of transcription factor functional equivalence: are Eyeless and Pax6 functionally equivalent or divergent? J Exp Zool B Mol Dev Evol 316B:93–98PubMedCrossRefGoogle Scholar
  70. Ma CY, Zhou Y, Beachy PA, Moses K (1993) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75:927–938PubMedCrossRefGoogle Scholar
  71. MacWhinnie SGB, Allee JP, Nelson CA, Riddiford LM, Truman JW, Champlin DT (2005) The role of nutrition in creation of the eye imaginal disc and initiation of metamorphosis in Manduca sexta. Dev Biol 285:285–297PubMedCrossRefGoogle Scholar
  72. Maderspacher F, Bucher G, Klingler M (1998) Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum. Dev Genes Evol 208:558–568PubMedCrossRefGoogle Scholar
  73. Mahfooz NS, Li H, Popadić A (2004) Differential expression patterns of the hox gene are associated with differential growth of insect hind legs. Proc Natl Acad Sci U S A 101:4877–4882PubMedCrossRefGoogle Scholar
  74. Maurel-Zaffran C, Treisman JE (2000) pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127:1007–1016PubMedGoogle Scholar
  75. Melzer RR, Paulus HF (1989) Evolutionswege zum Larvalauge der Insekten -Die Stemmata der höheren Dipteren und ihre Abwandlung zum Bolwig-Organ. Z Zool Syst Evolutionsforsch 27:200–245CrossRefGoogle Scholar
  76. Melzer RR, Michalke C, Smola U (2000) Walking on insect paths? Early ommatidial development in the compound eye of the ancestral crustacean, Triops cancriformis. Naturwissenschaften 87:308–311PubMedCrossRefGoogle Scholar
  77. Mito T, Noji S (2008) The two-spotted cricket Gryllus bimaculatus: an emerging model for developmental and regeneration studies. Cold Spring Harb Protoc: pdb.emo110Google Scholar
  78. Monsma SA, Booker R (1996) Genesis of the adult retina and outer optic lobes of the moth, Manduca sexta. I. patterns of proliferation and cell death. J Comp Neurol 367:10–20PubMedCrossRefGoogle Scholar
  79. Moreaux L, Laurent G (2007) Estimating firing rates from calcium signals in locust projection neurons in vivo. Front Neural Circuits 1:2PubMedCrossRefGoogle Scholar
  80. Moses K, Rodrigues AB (2004) Growth and specification: fly Pax6 homologs eyegone and eyeless have distinct functions. Bioessays 26:600–603PubMedCrossRefGoogle Scholar
  81. Müller C, Rosenberg J, Richter S, Meyer-Rochow V (2003) The compound eye of Scutigera coleoptrata (Linnaeus, 1758)(Chilopoda: Notostigmophora): an ultrastructural reinvestigation that adds support to the Mandibulata concept. Zoomorphology 122:191–209CrossRefGoogle Scholar
  82. Nilsson D-E (1996) Eye ancestry: old genes for new eyes. Curr Biol 6:39–42PubMedCrossRefGoogle Scholar
  83. Niwa N, Inoue Y, Nozawa A, Saito M, Misumi Y, Ohuchi H, Yoshioka H, Noji S (2000) Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development. Development 127:4373–4381PubMedGoogle Scholar
  84. Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034PubMedCrossRefGoogle Scholar
  85. Park T (1934) Observations on the general biology of the flour beetle, Tribolium confusum. Quart Rev Biol 9:36–64CrossRefGoogle Scholar
  86. Parthasarathy R, Tan A, Bai H, Palli SR (2008) Transcription factor broad suppresses precocious development of adult structures during larval–pupal metamorphosis in the red flour beetle, Tribolium castaneum. Mech Dev 125:299–313PubMedCrossRefGoogle Scholar
  87. Paterson JR, Garcia-Bellido DC, Lee MSY, Brock GA, Jago JB, Edgecombe GD (2011) Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480:237–240PubMedCrossRefGoogle Scholar
  88. Perez-Mendoza J, Campbell JF, Throne JE (2011) Effects of rearing density, age, sex, and food deprivation on flight initiation of the red flour beetle (Coleoptera: Tenebrionidae). J Econ Entomol 104:443–451PubMedCrossRefGoogle Scholar
  89. Perron M, Kanekar S, Vetter ML, Harris WA (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev Biol 199:185–200PubMedCrossRefGoogle Scholar
  90. Pichaud F, Casares F (2000) homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc. Mech Dev 96:15–25PubMedCrossRefGoogle Scholar
  91. Pichaud F, Desplan C (2002) Pax genes and eye organogenesis. Current Opionion in Genetics and. Development 12:430–434Google Scholar
  92. Posnien N, Schinko JB, Kittelmann S, Bucher G (2010) Genetics, development and composition of the insect head–a beetle’s view. Arthropod Struct Dev 39:399–410PubMedCrossRefGoogle Scholar
  93. Postlethwait JH, Schneiderman HA (1971) A clonal analysis of development in Drosophila melanogaster: morphogenesis, determination and and growth in the wild type antenna. Dev Biol 24:477–519PubMedCrossRefGoogle Scholar
  94. Prpic NM, Wigand B, Damen WG, Klingler M (2001) Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol 211:467–477PubMedCrossRefGoogle Scholar
  95. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 6:36PubMedCrossRefGoogle Scholar
  96. Reifegerste R, Moses K (1999) Genetics of epithelial polarity and pattern in the Drosophila retina. Bioessays 21:275–285PubMedCrossRefGoogle Scholar
  97. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Roth S, Schroder R, Tautz D, Zdobnov EM, Muzny D, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, Davis C, Chacko J, Dinh H, Dugan-Rocha S, Fowler G, Garner TT, Garnes J, Gnirke A, Hawes A, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Jackson L, Kovar C, Kowis A, Lee S, Lewis LR, Margolis J, Morgan M, Nazareth LV, Nguyen N, Okwuonu G, Parker D, Ruiz SJ, Santibanez J, Savard J, Scherer SE, Schneider B, Sodergren E, Vattahil S, Villasana D, White CS, Wright R, Park Y, Lord J, Oppert B, Brown S, Wang L, Weinstock G, Liu Y, Worley K, Elsik CG, Reese JT, Elhaik E, Landan G, Graur D, Arensburger P, Atkinson P, Beidler J, Demuth JP, Drury DW, Du YZ, Fujiwara H, Maselli V, Osanai M, Robertson HM, Tu Z, Wang JJ, Wang S, Song H, Zhang L, Werner D, Stanke M, Morgenstern B, Solovyev V, Kosarev P, Brown G, Chen HC, Ermolaeva O, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Maglott D, Pruitt K, Sapojnikov V, Souvorov A, Mackey AJ, Waterhouse RM, Wyder S, Kriventseva EV, Kadowaki T, Bork P, Aranda M, Bao R, Beermann A, Berns N, Bolognesi R, Bonneton F, Bopp D, Butts T, Chaumot A, Denell RE, Ferrier DE, Gordon CM, Jindra M, Lan Q, Lattorff HM, Laudet V, von Levetsow C, Liu Z, Lutz R, Lynch JA, da Fonseca RN, Posnien N, Reuter R, Schinko JB, Schmitt C, Schoppmeier M, Shippy TD, Simonnet F, Marques-Souza H, Tomoyasu Y, Trauner J, Van der Zee M, Vervoort M, Wittkopp N, Wimmer EA, Yang X, Jones AK, Sattelle DB, Ebert PR, Nelson D, Scott JG, Muthukrishnan S, Kramer KJ, Arakane Y, Zhu Q, Hogenkamp D, Dixit R, Jiang H, Zou Z, Marshall J, Elpidina E, Vinokurov K, Oppert C, Evans J, Lu Z, Zhao P, Sumathipala N, Altincicek B, Vilcinskas A, Williams M, Hultmark D, Hetru C, Hauser F, Cazzamali G, Williamson M, Li B, Tanaka Y, Predel R, Neupert S, Schachtner J, Verleyen P, Raible F, Walden KK, Angeli S, Foret S, Schuetz S, Maleszka R, Miller SC, Grossmann D (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955PubMedCrossRefGoogle Scholar
  98. Ridley AW, Hereward JP, Daglish GJ, Raghu S, Collins PJ, Walter GH (2011) The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and gene flow. Mol Ecol 20:1635–1646PubMedCrossRefGoogle Scholar
  99. Rogers SM, Harston GW, Kilburn-Toppin F, Matheson T, Burrows M, Gabbiani F, Krapp HG (2010) Spatiotemporal receptive field properties of a looming-sensitive neuron in solitarious and gregarious phases of the desert locust. J Neurophysiol 103:779–792PubMedCrossRefGoogle Scholar
  100. Roonwal ML (1936) Studies on the embryology of the African migratory locust, Locusta migratoria migratorioides Reiche and Frm. (Orthoptera, Acrididae) II-Organogeny. Philos Trans R Soc Lond B 227:175–244Google Scholar
  101. Salvini-Plawen L, Mayr E (1977) On the evolution of photoreceptors and eyes. Evol Biol 10:207–263CrossRefGoogle Scholar
  102. Sanchez D, Ganfornina MD, Bastiani M (1995) Contributions of an orthopteran to the understanding of neuronal pathfinding. Immunol Cell Biol 73:565–574PubMedCrossRefGoogle Scholar
  103. Sato K, Matsunaga TM, Futahashi R, Kojima T, Mita K, Banno Y, Fujiwara H (2008) Positional cloning of a Bombyx wingless locus flugellos (fl) reveals a crucial role for fringe that is specific for wing morphogenesis. Genetics 179:875–885PubMedCrossRefGoogle Scholar
  104. Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ (2006) Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of holometabolous insects. Genome Res 16:1334–1338PubMedCrossRefGoogle Scholar
  105. Schinko J, Hillebrand K, Bucher G (2012) Heat shock-mediated misexpression of genes in the beetle Tribolium castaneum. Dev Genes Evol 222:287–298PubMedCrossRefGoogle Scholar
  106. Schroder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621–625PubMedCrossRefGoogle Scholar
  107. Singh A, Kango-Singh M, Parthasarathy R, Gopinathan KP (2007) Larval legs of mulberry silkworm Bombyx mori are prototypes for the adult legs. Genesis 45:169–176PubMedCrossRefGoogle Scholar
  108. Smith WC, Price DA, Greenberg RM, Battelle BA (1993) Opsins from the lateral eyes and ocelli of the horseshoe-crab, Limulus polyphemus. Proc Natl Acad Sci U S A 90:6150–6154.PubMedCrossRefGoogle Scholar
  109. Sokoloff A (1972) The biology of Tribolium. Clarendon Press, OxfordGoogle Scholar
  110. Stambolic V, Ruel L, Woodgett JR (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 6:1664–1668PubMedCrossRefGoogle Scholar
  111. Suzuki Y, Truman JW, Riddiford LM (2008) The role of Broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development 135:569–577PubMedCrossRefGoogle Scholar
  112. Suzuki Y, Squires DC, Riddiford LM (2009) Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum. Dev Biol 326:60–67PubMedCrossRefGoogle Scholar
  113. Takagi A, Kurita K, Terasawa T, Nakamura T, Bando T, Moriyama Y, Mito T, Noji S, Ohuchi H (2012) Functional analysis of the role of eyes absent and sine oculis in the developing eye of the cricket Gryllus bimaculatus. Dev Growth Differ 54:227–240PubMedCrossRefGoogle Scholar
  114. Towner P, Harris P, Wolstenholme AJ, Hill C, Worm K, Gartner W (1997) Primary structure of locust opsins: a speculative model which may account for ultraviolet wavelength light detection. Vision Res 37:495–503PubMedCrossRefGoogle Scholar
  115. Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527PubMedGoogle Scholar
  116. Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500PubMedCrossRefGoogle Scholar
  117. Truman JW, Hiruma K, Allee JP, MacWhinnie SGB, Champlin DT, Riddiford LM (2006) Juvenile hormone is required to couple imaginal disc formation with nutrition in insects. Science 312:1385–1388PubMedCrossRefGoogle Scholar
  118. Uhlirova M, Foy BD, Beaty BJ, Olson KE, Riddiford LM, Jindra M (2003) Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc Natl Acad Sci U S A 100:15607–15612PubMedCrossRefGoogle Scholar
  119. Vishnevskaya TM, Cherkasov AD, Shura-Bura TM (1985) Spectral sensitivity of photoreceptors in the compound eye of the locust. Neurophysiology 18:69–76Google Scholar
  120. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, Winterton SL, Yeates DK (2009) Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol 7:34PubMedCrossRefGoogle Scholar
  121. Wieschaus E, Gehring W (1976) Clonal analysis of primordial disc cells in the early embryo of Drosophila melanogaster. Dev Biol 50:249–263PubMedCrossRefGoogle Scholar
  122. Wilson M, Garrard P, McGinness S (1978) The unit structure of the locust compound eye. Cell Tiss Res 195:205–226Google Scholar
  123. Yang X, Weber M, ZarinKamar N, Wigand B, Posnien G, Friedrich R, Beutel R, Damen W, Bucher G, Klingler M, Friedrich M (2009a) Probing the Drosophila retinal determination gene network in Tribolium (II): the Pax6 genes eyeless and twin of eyeless. Dev Biol 333:215–227CrossRefGoogle Scholar
  124. Yang X, ZarinKamar N, Bao R, Friedrich M (2009b) Probing the Drosophila retinal determination gene network in Tribolium (I): the early retinal genes dachshund, eyes absent and sine oculis. Dev Biol 333:202–214CrossRefGoogle Scholar
  125. Yu L, Zhou Q, Zhang C, Pignoni F (2012) Identification of Bombyx atonal and functional comparison with the Drosophila atonal proneural factor in the developing fly eye. Genesis 50:393–403PubMedCrossRefGoogle Scholar
  126. ZarinKamar N, Yang X, Bao R, Friedrich F, Beutel R, Friedrich M, 2011. The Pax gene eyegone facilitates repression of eye development in Tribolium. Evodevo 2:8PubMedCrossRefGoogle Scholar
  127. Zuker CS (1994) On the evolution of eyes: would you like it simple or compound? Science 265:742–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Markus Friedrich
    • 1
    • 2
    Email author
  • Ying Dong
    • 3
  • Zhenyi Liu
    • 4
  • Iris Yang
    • 1
  1. 1.Department of Biological SciencesWayne State UniversityDetroitUSA
  2. 2.Department of Anatomy and Cell BiologySchool of Medicine, Wayne State UniversityDetroitUSA
  3. 3.Harold C. Simmons Cancer CenterUT Southwestern Medical Center at DallasDallasUSA
  4. 4.Washington UniversitySt. LouisUSA

Personalised recommendations