Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

  • Elizabeth L. JockuschEmail author
  • Frank W. Smith


Arthropods are the most species-rich phylum. Within arthropods, species diversity is concentrated in the Hexapoda, which includes on the order of one million described species. The ancestor of hexapods was among the first metazoan lineages to move into a terrestrial environment. Hexapods were also the first lineage to evolve powered flight and remain the only invertebrate lineage to have done so. Hexapods are both exceptionally abundant in many habitats and exceptionally diverse ecologically, with lifestyles ranging from parasitic to agricultural. They also show extensive coevolutionary histories with other taxa, especially flowering plants, which hexapods both pollinate and consume. All of this diversity is achieved within a highly conserved body plan consisting of a segmented head, thorax, and abdomen, which bear an assortment of jointed appendages.



We appreciate feedback on drafts of this manuscript from Andreas Wanninger, Ariel Chipman, and Bernard Goffinet. Andreas Wanninger also provided extensive guidance about the project, along with nearly endless patience and encouragement. The other hexapod chapter authors, Volker Hartenstein and Ariel Chipman, graciously shared drafts of their manuscripts. We thank Doug Emlen, Julia Bowsher, and David Wagner for generously contributing photographs.


  1. Abouheif E, Wray GA (2002) Evolution of the gene network underlying wing polyphenism in ants. Science 297:249–252PubMedGoogle Scholar
  2. Abu-Shaar M, Mann RS (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125:3821–3830PubMedGoogle Scholar
  3. Abzhanov A, Kaufman TC (2000) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227:673–689PubMedGoogle Scholar
  4. Abzhanov A, Holtzman S, Kaufman TC (2001) The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes. Development 128:2803–2814PubMedGoogle Scholar
  5. Agata K, Saito Y, Nakajima E (2007) Unifying principles of regeneration I: epimorphosis versus morphallaxis. Dev Growth Differ 49:73–78PubMedGoogle Scholar
  6. Ahn Y, Zou J, Mitchell PJ (2011) Segment-specific regulation of the Drosophila AP-2 gene during leg and antennal development. Dev Biol 355:336–348PubMedCentralPubMedGoogle Scholar
  7. Akam ME (1983) The location of Ultrabithorax transcripts in Drosophila tissue sections. EMBO J 2:2075–2084PubMedCentralPubMedGoogle Scholar
  8. Akam M (1998) Hox genes: from master genes to micromanagers. Curr Biol 8:R676–R678PubMedGoogle Scholar
  9. Akam ME, Martinez-Arias A (1985) The distribution of Ultrabithorax transcripts in Drosophila embryos. EMBO J 4:1689–1700PubMedCentralPubMedGoogle Scholar
  10. Aldaz S, Escudero LM, Freeman M (2010) Live imaging of Drosophila imaginal disc development. Proc Natl Acad Sci 107:14217–14222PubMedCentralPubMedGoogle Scholar
  11. Alexandre C, Baena-Lopez A, Vincent J-P (2014) Patterning and growth control by membrane-tethered Wingless. Nature 505:180–185PubMedGoogle Scholar
  12. Ando T, Kojima T, Fujiwara H (2011) Dramatic changes in patterning gene expression during metamorphosis are associated with the formation of a feather-like antenna by the silk moth, Bombyx mori. Dev Biol 357:53–63PubMedGoogle Scholar
  13. Angelini DR, Kaufman TC (2004) Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects. Dev Biol 271:306–321PubMedGoogle Scholar
  14. Angelini DR, Kaufman TC (2005) Functional analyses in the milkweed bug Oncopeltus fasciatus (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. Dev Biol 283:409–423PubMedGoogle Scholar
  15. Angelini DR, Liu PZ, Hughes CL, Kaufman TC (2005) Hox gene function and interaction in the milkweed bug Oncopeltus fasciatus (Hemiptera). Dev Biol 287:440–455PubMedGoogle Scholar
  16. Angelini DR, Kikuchi M, Jockusch EL (2009) Genetic patterning in the adult capitate antenna of the beetle Tribolium castaneum. Dev Biol 327:240–251PubMedGoogle Scholar
  17. Angelini DR, Smith FW, Aspiras AC, Kikuchi M, Jockusch EL (2012a) Patterning of the adult mandibulate mouthparts in the red flour beetle, Tribolium castaneum. Genetics 190:639–654PubMedCentralPubMedGoogle Scholar
  18. Angelini DR, Smith FW, Jockusch EL (2012b) Extent with modification: leg patterning in the beetle Tribolium castaneum and the evolution of serial homologs. G3 Genes Genome Genet 2:235–248Google Scholar
  19. Aranda M (2006) Functional analysis of a homolog of the pair-rule gene hairy in the short-germ beetle Tribolium castaneum. Inaugural-Dissertation, Universität zu KölnGoogle Scholar
  20. Aranda M, Marques-Souza H, Bayer T, Tautz D (2008) The role of the segmentation gene hairy in Tribolium. Dev Genes Evol 218:465–477PubMedCentralPubMedGoogle Scholar
  21. Arnoult L, Su KFY, Manoel D, Minervino C, Magrina J, Gompel N, Prud’homme B (2013) Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339:1423–1426PubMedGoogle Scholar
  22. Aspiras AC, Smith FW, Angelini DR (2011) Sex-specific gene interactions in the patterning of insect genitalia. Dev Biol 360:369–380PubMedGoogle Scholar
  23. Atallah J, Vurens G, Mavong S, Mutti A, Hoang D, Kopp A (2014) Sex-specific repression of dachshund is required for Drosophila sex comb development. Dev Biol 386:440–447PubMedGoogle Scholar
  24. Averof M, Cohen SM (1997) Evolutionary origin of insect wings from ancestral gills. Nature 385:627–630PubMedGoogle Scholar
  25. Ayala-Camargo A, Anderson AM, Amoyel M, Rodrigues AB, Flaherty MS, Bach EA (2013) JAK/STAT signaling is required for hinge growth and patterning in the Drosophila wing disc. Dev Biol 382:413–426PubMedCentralPubMedGoogle Scholar
  26. Azpiazu N, Morata G (2000) Function and regulation of homothorax in the wing imaginal disc of Drosophila. Development 127:2685–2693PubMedGoogle Scholar
  27. Baanannou A, Mojica-Vazquez LH, Darras G, Couderc J-L, Cribbs DL, Boube M, Bourbon H-M (2013) Drosophila Distal-less and Rotund bind a single enhancer ensuring reliable and robust bric-a-brac2 expression in distinct limb morphogenetic fields. PLoS Genet 9:e1003581PubMedCentralPubMedGoogle Scholar
  28. Bando T, Mito T, Maeda Y, Nakamura T, Ito F, Watanabe T, Ohuchi H, Noji S (2009) Regulation of leg size and shape by the Dachsous/Fat signalling pathway during regeneration. Development 136:2235–2245PubMedGoogle Scholar
  29. Bando T, Ishimaru Y, Kida T, Hamada Y, Matsuoka Y, Nakamura T, Ohuchi H, Noji S, Mito T (2013) Analysis of RNA-Seq data reveals involvement of JAK/STAT signalling during leg regeneration in the cricket Gryllus bimaculatus. Development 140:959–964PubMedGoogle Scholar
  30. Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368:208–214PubMedGoogle Scholar
  31. Bate CM (1976) Embryogenesis of an insect nervous system I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. J Embryol Exp Morphol 35:107–123PubMedGoogle Scholar
  32. Beeman RW (1987) A homoeotic gene cluster in the red flour beetle. Nature 327:247–249Google Scholar
  33. Beeman RW, Stuart JJ, Haas MS, Denell RE (1989) Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. Dev Biol 133:196–209PubMedGoogle Scholar
  34. Beeman RW, Stuart JJ, Brown SJ, Denell RE (1993) Structure and function of the homeotic gene complex (HOM-C) in the beetle, Tribolium castaneum. Bioessays 15:439–444PubMedGoogle Scholar
  35. Beermann A, Schröder R (2004) Functional stability of the aristaless gene in appendage tip formation during evolution. Dev Genes Evol 214:303–308PubMedGoogle Scholar
  36. Beermann A, Jay DG, Beeman RW, Hulskamp M, Tautz D, Jürgens G (2001) The Short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein. Development 128:287–297PubMedGoogle Scholar
  37. Beermann A, Aranda M, Schröder R (2004) The Sp8 zinc-finger transcription factor is involved in allometric growth of the limbs in the beetle Tribolium castaneum. Development 131:733–742PubMedGoogle Scholar
  38. Beermann A, Pruhs R, Lutz R, Schroder R (2011) A context-dependent combination of Wnt receptors controls axis elongation and leg development in a short germ insect. Development 138:2793–2805PubMedCentralPubMedGoogle Scholar
  39. Bergantiños C, Corominas M, Serras F (2010) Cell death-induced regeneration in wing imaginal discs requires JNK signalling. Development 137:1169–1179PubMedGoogle Scholar
  40. Bergsten SE, Gavis ER (1999) Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development 126:659–669PubMedGoogle Scholar
  41. Berlese A (1913) Intorno alle metamorfosi degli insetti. Redia 9:121–136Google Scholar
  42. Berns N, Kusch T, Schröder R, Reuter R (2008) Expression, function and regulation of Brachyenteron in the short germband insect Tribolium castaneum. Dev Genes Evol 218:169–179PubMedGoogle Scholar
  43. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS (2002) Combinatorial control of Drosophila eye development by Eyeless, Homothorax, and Teashirt. Genes Dev 16:2415–2427PubMedCentralPubMedGoogle Scholar
  44. Biffar L, Stollewerk A (2014) Conservation and evolutionary modifications of neuroblast expression patterns in insects. Dev Biol 388:103–116PubMedGoogle Scholar
  45. Bishop SA, Klein T, Arias AM, Couso JP (1999) Composite signalling from Serrate and Delta establishes leg segments in Drosophila through Notch. Development 126:2993–3003PubMedGoogle Scholar
  46. Bitsch J (2012) The controversial origin of the abdominal appendage-like processes in immature insects: are they true segmental appendages or secondary outgrowths? (Arthropoda, Hexapoda). J Morphol 273:919–931PubMedGoogle Scholar
  47. Blair SS (2007) Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu Rev Cell Dev Biol 23:293–319PubMedGoogle Scholar
  48. Bolognesi R, Beermann A, Farzana L, Wittkopp N, Lutz R, Balavoine G, Brown SJ, Schröder R (2008a) Tribolium Wnts: evidence for a larger repertoire in insects with overlapping expression patterns that suggest multiple redundant functions in embryogenesis. Dev Genes Evol 218:193–202PubMedCentralPubMedGoogle Scholar
  49. Bolognesi R, Farzana L, Fischer TD, Brown SJ (2008b) Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 18:1624–1629PubMedCentralPubMedGoogle Scholar
  50. Bomtorin AD, Barchuk AR, Moda LM, Simoes ZLP (2012) Hox gene expression leads to differential hind leg development between honeybee castes. PLoS One 7:e40111PubMedCentralPubMedGoogle Scholar
  51. Borrell BJ, Krenn HW (2006) Nectar feeding in long-proboscis insects. In: Herrel A, Speck T, Rowe NP (eds) Ecology and biomechanics: a mechanical approach to the ecology and animals and plants. Taylor & Francis/CRC, Boca Raton, pp 185–212Google Scholar
  52. Bosch M, Serras F, Martin-Blanco E, Baguna J (2005) JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev Biol 280:73–86PubMedGoogle Scholar
  53. Bosch M, Bishop SA, Baguna J, Couso JP (2010) Leg regeneration in Drosophila abridges the normal developmental program. Int J Dev Biol 54:1241–1250PubMedCentralPubMedGoogle Scholar
  54. Bowsher JH, Nijhout HF (2007) Evolution of novel abdominal appendages in a sepsid fly from histoblasts, not imaginal discs. Evol Dev 9:347–354PubMedGoogle Scholar
  55. Bowsher JH, Nijhout HF (2009) Partial co-option of the appendage patterning pathway in the development of abdominal appendages in the sepsid fly Themira biloba. Dev Genes Evol 219:577–587PubMedCentralPubMedGoogle Scholar
  56. Bowsher JH, Ang Y, Ferderer T, Meier R (2013) Deciphering the evolutionary history and developmental mechanisms of a complex sexual ornament: the abdominal appendages of Sepsidae (Diptera): phylogeny and development of abdominal appendages. Evolution 67:1069–1080PubMedGoogle Scholar
  57. Boxshall GA (2004) The evolution of arthropod limbs. Biol Rev 79:253–300PubMedGoogle Scholar
  58. Brena C, Liu PZ, Minelli A, Kaufman TC (2005) Abd-B expression in Porcellio scaber Latreille, 1804 (Isopoda: Crustacea): conserved pattern versus novel roles in development and evolution. Evol Dev 7:42–50PubMedGoogle Scholar
  59. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510PubMedGoogle Scholar
  60. Brisson JA, Ishikawa A, Miura T (2010) Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs. Insect Mol Biol 19:63–73PubMedGoogle Scholar
  61. Broadus J, Doe CQ (1995) Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca. Development 121:3989–3996PubMedGoogle Scholar
  62. Brown S, Holtzman S, Kaufman T, Denell R (1999a) Characterization of the Tribolium Deformed ortholog and its ability to directly regulate Deformed target genes in the rescue of a Drosophila Deformed null mutant. Dev Genes Evol 209:389–398PubMedGoogle Scholar
  63. Brown SJ, Mahaffey JP, Lorenzen MD, Denell RE, Mahaffey JW (1999b) Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol Dev 1:11–15PubMedGoogle Scholar
  64. Brown SJ, Shippy TD, Beeman RW, Denell RE (2002) Tribolium Hox genes repress antennal development in the gnathos and trunk. Mol Phylogenet Evol 24:384–387PubMedGoogle Scholar
  65. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB (2001) The generation and diversification of butterfly eyespot color patterns. Curr Biol 11:1578–1585PubMedGoogle Scholar
  66. Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Associates, Sunderland, MAGoogle Scholar
  67. Bryant SV, French V, Bryant PJ (1981) Distal regeneration and symmetry. Science 212:993–1002PubMedGoogle Scholar
  68. Bryantsev AL, Cripps RM (2009) Cardiac gene regulatory networks in Drosophila. Biochim Biophys Acta (BBA) Gene Regul Mech 1789:343–353Google Scholar
  69. Buceta J, Herranz H, Canela-Xandri O, Reigada R, Sagués F, Milán M (2007) Robustness and stability of the gene regulatory network involved in DV boundary formation in the Drosophila wing. PLoS One 2:e602PubMedCentralPubMedGoogle Scholar
  70. Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85–R86PubMedGoogle Scholar
  71. Buschbeck EK, Friedrich M (2008) Evolution of insect eyes: tales of ancient heritage, deconstruction, reconstruction, remodeling, and recycling. Evol Educ Outreach 1:448–462Google Scholar
  72. Campbell G (2002) Distalization of the Drosophila leg by graded EGF-receptor activity. Nature 418:781–785PubMedGoogle Scholar
  73. Campbell G (2005) Regulation of gene expression in the distal region of the Drosophila leg by the Hox11 homolog, C15. Dev Biol 278:607–618PubMedGoogle Scholar
  74. Campbell LJ, Crews CM (2008) Wound epidermis formation and function in urodele amphibian limb regeneration. Cell Mol Life Sci 65:73–79PubMedGoogle Scholar
  75. Campbell G, Tomlinson A (1995) Initiation of the proximodistal axis in insect legs. Development 121:619–628Google Scholar
  76. Campbell G, Tomlinson A (1998) The roles of the homeobox genes aristaless and Distal-less in patterning the legs and wings of Drosophila. Development 125:4483–4493PubMedGoogle Scholar
  77. Campbell G, Weaver T, Tomlinson A (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74:1113–1123PubMedGoogle Scholar
  78. Cande JD, Chopra VS, Levine M (2009) Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum. Development 136:3153–3160PubMedCentralPubMedGoogle Scholar
  79. Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban GE, Selegue JE, Williams JA (1994) Pattern formation and eyespot determination in butterfly wings. Science 265:109–114PubMedGoogle Scholar
  80. Casares F, Mann RS (1998) Control of antennal versus leg development in Drosophila. Nature 392:723–726PubMedGoogle Scholar
  81. Casares F, Mann RS (2000) A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila. Development 127:1499–1508PubMedGoogle Scholar
  82. Casares F, Mann RS (2001) The ground state of the ventral appendage in Drosophila. Science 293:1477–1480PubMedGoogle Scholar
  83. 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 126:4933–4942Google Scholar
  84. Cavodeassi F, Modolell J, Gomez-Skarmeta JL (2001) The Iroquois family of genes: from body building to neural patterning. Development 128:2847–2855PubMedGoogle Scholar
  85. 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
  86. Chang C, Dearden P, Akam M (2002) Germ line development in the grasshopper Schistocerca gregaria: vasa as a marker. Dev Biol 252:100–118PubMedGoogle Scholar
  87. Chang C-C, Lee W-C, Cook CE, Lin G-W, Chang T (2006) Germ-plasm specification and germline development in the parthenogenetic pea aphid Acyrthosiphon pisum: vasa and Nanos as markers. Int J Dev Biol 50:413–421Google Scholar
  88. Chang C, Lin G, Cook CE, Horng S, Lee H, Huang T (2007) Apvasa marks germ-cell migration in the parthenogenetic pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Dev Genes Evol 217:275–287PubMedGoogle Scholar
  89. Chang C-C, Huang T-Y, Cook CE, Lin G-W, Shih C-L, Chen RP-Y (2009) Developmental expression of Apnanos during oogenesis and embryogenesis in the parthenogenetic pea aphid Acyrthosiphon pisum. Int J Dev Biol 53:169–176PubMedGoogle Scholar
  90. Chanut F, Heberlein U (1997) Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 124:559–567PubMedGoogle Scholar
  91. Chen R, Amoui M, Zhang Z, Mardon G (1997) Dachshund and Eyes Absent proteins form a complex and function synergistically to induce ectopic eye development in Drosophila. Cell 91:893–903PubMedGoogle Scholar
  92. Chen EH, Christiansen AE, Baker BS (2005) Allocation and specification of the genital disc precursor cells in Drosophila. Dev Biol 281:270–285PubMedGoogle Scholar
  93. Chen P, Tong X-L, Li D-D, Liang P-F, Fu M-Y, Li C-F, Hu H, Xiang Z-H, Lu C, Dai F-Y (2013) Fine mapping of a supernumerary proleg mutant (E Cs-l) and comparative expression analysis of the abdominal-A gene in silkworm, Bombyx mori: fine mapping of the silkworm E Cs-l locus. Insect Mol Biol 22:497–504PubMedGoogle Scholar
  94. Chesebro J (2013) Mechanisms of segmentation in the American cockroach, Periplaneta americana. D. Phil. Thesis. University of SussexGoogle Scholar
  95. Chesebro J, Hrycaj S, Mahfooz N, Popadić A (2009) Diverging functions of Scr between embryonic and post-embryonic development in a hemimetabolous insect, Oncopeltus fasciatus. Dev Biol 329:142–151PubMedCentralPubMedGoogle Scholar
  96. Cho K-O, Choi K-W (1998) Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature 396:272–276Google Scholar
  97. Cho K-O, Chern J, Izaddoost S, Choi K-W (2000) Novel signaling from the peripodial membrane is essential for eye disc patterning in Drosophila. Cell 103:331–342Google Scholar
  98. Chu J, Dong PS, Panganiban G (2002) Limb type-specific regulation of bric a brac contributes to morphological diversity. Development 129:695–704PubMedGoogle Scholar
  99. Clark-Hachtel CM, Linz DM, Tomoyasu Y (2013) Insights into insect wing origin provided by functional analysis of vestigial in the red flour beetle, Tribolium castaneum. Proc Natl Acad Sci 110:16951–16956PubMedCentralPubMedGoogle Scholar
  100. Cohen SM (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343:173–177PubMedGoogle Scholar
  101. Cohen SM, Jürgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482–485PubMedGoogle Scholar
  102. Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–272PubMedGoogle Scholar
  103. Cohen B, Simcox AA, Cohen SM (1993) Allocation of the thoracic imaginal primordia in the Drosophila embryo. Development 117:597–608PubMedGoogle Scholar
  104. Coulcher JF, Telford MJ (2012) Capncollar differentiates the mandible from the maxilla in the beetle Tribolium castaneum. EvoDevo 3:25PubMedCentralPubMedGoogle Scholar
  105. Coulcher JF, Telford MJ (2013) Comparative gene expression supports the origin of the incisor and molar process from a single endite in the mandible of the red flour beetle Tribolium castaneum. EvoDevo 4:1PubMedCentralPubMedGoogle Scholar
  106. Crampton GC (1916) The phylogenetic origin and the nature of the wings of insects according to the paranotal theory. J N Y Entomol Soc 24:1–38Google Scholar
  107. Curtis CD, Brisson JA, DeCamillis MA, Shippy TD, Brown SJ, Denell RE (2001) Molecular characterization of Cephalothorax, the Tribolium ortholog of Sex combs reduced. Genesis 30:12–20PubMedGoogle Scholar
  108. Czerny T, Halder G, Kloter U, Souabni A, Gehring WJ, Busslinger M (1999) twin of eyeless, a second Pax-6 gene of Drosophila, acts upstream of eyeless in the control of eye development. Mol Cell 3:297–307PubMedGoogle Scholar
  109. de Celis Ibeas JM, Bray SJ (2003) Bowl is required downstream of Notch for elaboration of distal limb patterning. Development 130:5943–5952PubMedGoogle Scholar
  110. de Celis JF, Diaz-Benjumea FJ (2003) Developmental basis for vein pattern variations in insect wings. Int J Dev Biol 47:653–664PubMedGoogle Scholar
  111. de Celis JF, Tyler DM, de Celis J, Bray SJ (1998) Notch signalling mediates segmentation of the Drosophila leg. Development 125:4617–4626PubMedGoogle Scholar
  112. Dearden PK (2006) Germ cell development in the honeybee (Apis mellifera); Vasa and Nanos expression. BMC Dev Biol 6:6PubMedCentralPubMedGoogle Scholar
  113. Dearden P, Akam M (2000) A role for Fringe in segment morphogenesis but not segment formation in the grasshopper, Schistocerca gregaria. Dev Genes Evol 210:329–336PubMedGoogle Scholar
  114. DeCamillis MA, ffrench-Constant R (2003) Proboscipedia represses distal signaling in the embryonic gnathal limb fields of Tribolium castaneum. Dev Genes Evol 213:55–64PubMedGoogle Scholar
  115. DeCamillis MA, Lewis DL, Brown SJ, Beeman RW, Denell RE (2001) Interactions of the Tribolium Sex combs reduced and proboscipedia orthologs in embryonic labial development. Genetics 159:1643–1648PubMedCentralPubMedGoogle Scholar
  116. Demontis F, Dahmann C (2007) Apical and lateral cell protrusions interconnect epithelial cells in live Drosophila wing imaginal discs. Dev Dyn 236:3408–3418PubMedGoogle Scholar
  117. Desplan C (1997) Eye development: governed by a dictator or a junta? Cell 91:861–864PubMedGoogle Scholar
  118. Diaz-Benjumea FJ, Cohen SM (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75:741–752PubMedGoogle Scholar
  119. Diaz-Benjumea FJ, Cohen SM (1995) Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121:4215–4225Google Scholar
  120. Diaz-Benjumea FJ, Cohen B, Cohen SM (1994) Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs. Nature 372:175–179PubMedGoogle Scholar
  121. Doe CQ (1992) Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116:855–863PubMedGoogle Scholar
  122. Doe CQ, Goodman CS (1985a) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205PubMedGoogle Scholar
  123. Doe CQ, Goodman CS (1985b) Early events in insect neurogenesis: II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol 111:206–219PubMedGoogle Scholar
  124. Domínguez M, de Celis JF (1998) A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396:276–278PubMedGoogle Scholar
  125. Dong Y, Friedrich M (2005) Nymphal RNAi: systemic RNAi mediated gene knockdown in juvenile grasshopper. BMC Biotechnol 5:25PubMedCentralPubMedGoogle Scholar
  126. Dong PDS, Chu J, Panganiban G (2000) Coexpression of the homeobox genes Distal-less and homothorax determines Drosophila antennal identity. Development 127:209–216PubMedGoogle Scholar
  127. Dong PDS, Chu J, Panganiban G (2001) Proximodistal domain specification and interactions in developing Drosophila appendages. Development 128:2365–2372PubMedGoogle Scholar
  128. Dong PDS, Dicks JS, Panganiban G (2002) Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna. Development 129:1967–1974PubMedGoogle Scholar
  129. Donnell DM, Strand MR (2006) Caste-based differences in gene expression in the polyembryonic wasp Copidosoma floridanum. Insect Biochem Mol Biol 36:141–153PubMedGoogle Scholar
  130. Donnell DM, Corley LS, Chen G, Strand MR (2004) Caste determination in a polyembryonic wasp involves inheritance of germ cells. Proc Natl Acad Sci U S A 101:10095–10100PubMedCentralPubMedGoogle Scholar
  131. Donoughe S, Nakamura T, Ewen-Campen B, Green DA, Henderson L, Extavour CG (2014) BMP signaling is required for the generation of primordial germ cells in an insect. Proc Natl Acad Sci U S A 111:4133–4138PubMedCentralPubMedGoogle Scholar
  132. Doumpas N, Jékely G, Teleman AA (2013) Wnt6 is required for maxillary palp formation in Drosophila. BMC Biol 11:104PubMedCentralPubMedGoogle Scholar
  133. Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560PubMedGoogle Scholar
  134. Duncan DM, Burgess EA, Duncan I (1998) Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev 12:1290–1303PubMedCentralPubMedGoogle Scholar
  135. Duncan D, Kiefel P, Duncan I (2010) Control of the spineless antennal enhancer: direct repression of antennal target genes by Antennapedia. Dev Biol 347:82–91PubMedCentralPubMedGoogle Scholar
  136. Durston AJ, Jansen HJ, In der Rieden P, Hooiveld MH (2011) Hox collinearity – a new perspective. Int J Dev Biol 55:899–908PubMedGoogle Scholar
  137. Edwards KA, Doescher LT, Kaneshiro KY, Yamamoto D (2007) A database of wing diversity in the Hawaiian Drosophila. PLoS One 2:e487PubMedCentralPubMedGoogle Scholar
  138. Ekas LA, Baeg GH, Flaherty MS, Ayala-Camargo A, Bach EA (2006) JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133:4721–4729PubMedGoogle Scholar
  139. Emerald BS, Curtiss J, Mlodzik M, Cohen SM (2003) distal antenna and distal antenna related encode nuclear proteins containing pipsqueak motifs involved in antenna development in Drosophila. Development 130:1171–1180PubMedGoogle Scholar
  140. Emlen DJ, Warren IA, Johns A, Dworkin I, Lavine LC (2012) A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337:860–864PubMedGoogle Scholar
  141. Emmons RB, Duncan D, Duncan I (2007) Regulation of the Drosophila distal antennal determinant spineless. Dev Biol 302:412–426PubMedCentralPubMedGoogle Scholar
  142. Erezyilmaz DF (2006) Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis. Integr Comp Biol 46:795–807PubMedGoogle Scholar
  143. Erezyilmaz D, Riddiford L, Truman J (2004) Juvenile hormone acts at embryonic molts and induces the nymphal cuticle in the direct-developing cricket. Dev Genes Evol 214:313–323PubMedGoogle Scholar
  144. Estella C, Mann RS (2008) Logic of Wg and Dpp induction of distal and medial fates in the Drosophila leg. Development 135:627–636PubMedCentralPubMedGoogle Scholar
  145. Estella C, Mann RS (2010) Non-redundant selector and growth-promoting functions of two sister genes, buttonhead and Sp1, in Drosophila leg development. PLoS Genet 6:e1001001PubMedCentralPubMedGoogle Scholar
  146. Estella C, Voutev R, Mann RS (2012) A dynamic network of morphogens and transcription factors patterns the fly leg. Curr Top Dev Biol 98:173–198PubMedCentralPubMedGoogle Scholar
  147. Estrada B, Sánchez-Herrero E (2001) The Hox gene Abdominal-B antagonizes appendage development in the genital disc of Drosophila. Development 128:331–339PubMedGoogle Scholar
  148. Ewen-Campen B, Srouji JR, Schwager EE, Extavour CG (2012) oskar predates the evolution of germ plasm in insects. Curr Biol 22:2278–2283PubMedGoogle Scholar
  149. Ewen-Campen B, Jones TEM, Extavour CG (2013a) Evidence against a germ plasm in the milkweed bug Oncopeltus fasciatus, a hemimetabolous insect. Biol Open 2:556–568PubMedCentralPubMedGoogle Scholar
  150. Ewen-Campen B, Donoughe S, Clarke DN, Extavour CG (2013b) Germ cell specification requires zygotic mechanisms rather than germ plasm in a basally branching insect. Curr Biol 23:835–842PubMedGoogle Scholar
  151. Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884PubMedGoogle Scholar
  152. Feltwell J, Rothschild M (1974) Carotenoids in thirty-eight species of Lepidoptera. J Zool 174:441–465Google Scholar
  153. Foronda D, Estrada B, de Navas L, Sánchez-Herrero E (2006) Requirement of abdominal-A and Abdominal-B in the developing genitalia of Drosophila breaks the posterior downregulation rule. Development 133:182–182Google Scholar
  154. French V (1976) Leg regeneration in the cockroach, Blatella germanica. II. Regeneration from a non-congruent tibial graft/host junction. J Embryol Exp Morphol 35:267–301Google Scholar
  155. Friedrich M (2006a) Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila. Arthropod Struct Dev 35:357–378PubMedGoogle Scholar
  156. Friedrich M (2006b) Continuity versus split and reconstitution: exploring the molecular developmental corollaries of insect eye primordium evolution. Dev Biol 299:310–329PubMedGoogle Scholar
  157. Friedrich M, Benzer S (2000) Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis. J Exp Zool 288:39–55PubMedGoogle Scholar
  158. Friedrich M, Dong Y, Liu Z, Yang I (2013) Genetic regulation of early eye development in non-dipteran insects. In: Singh A, Kango-Singh M (eds) Molecular genetics of axial patterning, growth and disease in the Drosophila eye. Springer, New YorkGoogle Scholar
  159. Fristrom D, Gotwals P, Eaton S, Kornberg TB, Sturtevant M, Bier E, Fristrom JW (1994) blistered: a gene required for vein/intervein formation in wings of Drosophila. Development 120:2661–2671PubMedGoogle Scholar
  160. Fujii T, Abe H, Katsuma S, Shimada T (2011) Identification and characterization of the fusion transcript, composed of the apterous homolog and a putative protein phosphatase gene, generated by 1.5-Mb interstitial deletion in the vestigial (Vg) mutant of Bombyx mori. Insect Biochem Mol Biol 41:306–312PubMedGoogle Scholar
  161. Galant R, Carroll SB (2002) Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415:910–913PubMedGoogle Scholar
  162. Galant R, Skeath JB, Paddock S, Lewis DL, Carroll SB (1998) Expression pattern of a butterfly achaete-scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Curr Biol 8:807–813PubMedGoogle Scholar
  163. Galindo MI, Bishop SA, Greig S, Couso JP (2002) Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 297:256–259PubMedGoogle Scholar
  164. Galindo MI, Bishop SA, Couso JP (2005) Dynamic EGFR-Ras signalling in Drosophila leg development. Dev Dyn 233:1496–1508PubMedGoogle Scholar
  165. Galindo MI, Fernández-Garza D, Phillips R, Couso JP (2011) Control of Distal-less expression in the Drosophila appendages by functional 3′ enhancers. Dev Biol 353:396–410PubMedCentralPubMedGoogle Scholar
  166. Gallant JR, Imhoff VE, Martin A, Savage WK, Chamberlain NL, Pote BL, Peterson C, Smith GE, Evans B, Reed RD, Kronforst MR, Mullen SP (2014) Ancient homology underlies adaptive mimetic diversity across butterflies. Nat Commun 5:4817PubMedCentralPubMedGoogle Scholar
  167. Gibson MC, Schubiger G (1999) Hedgehog is required for activation of engrailed during regeneration of fragmented Drosophila imaginal discs. Development 126:1591–1599PubMedGoogle Scholar
  168. Gibson MC, Schubiger G (2000) Peripodial cells regulate proliferation and patterning of Drosophila imaginal discs. Cell 103:343–350PubMedGoogle Scholar
  169. Giorgianni MW, Mann RS (2011) Establishment of medial fates along the proximodistal axis of the Drosophila leg through direct activation of dachshund by Distalless. Dev Cell 20:455–468PubMedCentralPubMedGoogle Scholar
  170. Giorgianni MW, Patel NH (2004) Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol Dev 6:402–410PubMedGoogle Scholar
  171. Godt D, Couderc J-L, Cramton SE, Laski FA (1993) Pattern in the limbs of Drosophila: bric à brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus. Development 119:799–812PubMedGoogle Scholar
  172. Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433:481–487PubMedGoogle Scholar
  173. González-Crespo S, Morata G (1995) Control of Drosophila adult pattern by extradenticle. Development 121:2117–2125PubMedGoogle Scholar
  174. Gordon SD, Strand MR (2009) The polyembryonic wasp Copidosoma floridanum produces two castes by differentially parceling the germ line to daughter embryos during embryo proliferation. Dev Genes Evol 219:445–454PubMedGoogle Scholar
  175. Grbić M, Nagy LM, Strand MR (1998) Development of polyembryonic insects: a major departure from typical insect embryogenesis. Dev Genes Evol 208:69–81PubMedGoogle Scholar
  176. Greenberg L, Hatini V (2009) Essential roles for lines in mediating leg and antennal proximodistal patterning and generating a stable Notch signaling interface at segment borders. Dev Biol 330:93–104PubMedCentralPubMedGoogle Scholar
  177. 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
  178. Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, CambridgeGoogle Scholar
  179. Grossmann D, Prpic N-M (2012) Egfr signaling regulates distal as well as medial fate in the embryonic leg of Tribolium castaneum. Dev Biol 370:264–272PubMedGoogle Scholar
  180. Grossmann D, Scholten J, Prpic N-M (2009) Separable functions of wingless in distal and ventral patterning of the Tribolium leg. Dev Genes Evol 219:469–479PubMedCentralPubMedGoogle Scholar
  181. Guarner A, Manjón C, Edwards K, Steller H, Suzanne M, Sánchez-Herrero E (2014) The zinc finger homeodomain-2 gene of Drosophila controls Notch targets and regulates apoptosis in the tarsal segments. Dev Biol 385:350–365PubMedGoogle Scholar
  182. Gurley KA, Rink JC, Alvarado AS (2008) β-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319:323–327PubMedCentralPubMedGoogle Scholar
  183. Gustafson EA, Wessel GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. Bioessays 32:626–637PubMedCentralPubMedGoogle Scholar
  184. Hamilton KGA (1972) The insect wing, part III. Venation of the orders. J Kansas Entomol Soc 45:145–162Google Scholar
  185. Hao I, Green RB, Dunaevsky O, Lengyel JA, Rauskolb C (2003) The odd-skipped family of zinc finger genes promotes Drosophila leg segmentation. Dev Biol 263:282–295PubMedGoogle Scholar
  186. Hartenstein V, Rudloff E, Campos-Ortega JA (1987) The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster. Roux’s Arch Dev Biol 196:473–485Google Scholar
  187. Hayashi S, Hirose S, Metcalfe T, Shirras AD (1993) Control of imaginal cell development by the escargot gene of Drosophila. Development 118:105–115PubMedGoogle Scholar
  188. Hayashi Y, Hayashi M, Kobayashi S (2004) Nanos suppresses somatic cell fate in Drosophila germ line. Proc Natl Acad Sci U S A 101:10338–10342PubMedCentralPubMedGoogle Scholar
  189. Heberlein U, Wolff T, Rubin GM (1993) The TGFβ homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina. Cell 75:913–926PubMedGoogle Scholar
  190. Heffer A, Pick L (2013) Conservation and variation in Hox genes: how insect models pioneered the evo-devo field. Annu Rev Entomol 58:161–179PubMedGoogle Scholar
  191. Heliconius Genome Consortium (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:94–98Google Scholar
  192. Hinton HE (1948) On the origin and function of the pupal stage. Trans R Entomol Soc Lond 99:395–409Google Scholar
  193. Hinton HE (1963) The origin and function of the pupal stage. Proc R Entomol Soc Lond Ser A Gen Entomol 38:77–85Google Scholar
  194. Hoch H, Wessel A, Asche M, Baum D, Beckmann F, Bräunig P, Ehrig K, Mühlethaler R, Riesemeier H, Staude A, Stelbrink B, Wachmann E, Weintraub P, Wipfler B, Wolff C, Zilch M (2014) Non-sexual abdominal appendages in adult insects challenge a 300 million year old bauplan. Curr Biol 24:R16–R17PubMedGoogle Scholar
  195. Horváth G, Varjú D (2004) Polarized light in animal vision: polarization patterns in nature. Springer, New YorkGoogle Scholar
  196. Hrycaj S, Mihajlovic M, Mahfooz N, Couso JP, Popadić A (2008) RNAi analysis of nubbin embryonic functions in a hemimetabolous insect, Oncopeltus fasciatus. Evol Dev 10:705–716PubMedGoogle Scholar
  197. Hrycaj S, Chesebro J, Popadić A (2010) Functional analysis of Scr during embryonic and post-embryonic development in the cockroach, Periplaneta americana. Dev Biol 341:324–334PubMedCentralPubMedGoogle Scholar
  198. Huet PC, Lenoir-Rousseaux JJ (1976) Etude de la mise en place de la patte imaginale de Tenebrio molitor. 1. Analyse expérimentale des processus de restauration au cours de la morphogenése. J Embryol Exp Morphol 35:303–321PubMedGoogle Scholar
  199. Hughes CL, Kaufman TC (2000) RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the Hemipteran head. Development 127:3683–3694PubMedGoogle Scholar
  200. Hughes CL, Kaufman TC (2002) Hox genes and the evolution of the arthropod body plan. Evol Dev 4:459–499PubMedGoogle Scholar
  201. Hughes CL, Liu PZ, Kaufman TC (2004) Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol Dev 6:393–401PubMedGoogle Scholar
  202. Imms AD (1931) Recent advances in entomology. J. & A. Churchill, LondonGoogle Scholar
  203. Inoue Y, Mito T, Miyawaki K, Matsushima K, Shinmyo Y, Heanue TA, Mardon G, Ohuchi H, Noji S (2002a) Correlation of expression patterns of homothorax, dachshund, and Distal-less with the proximodistal segmentation of the cricket leg bud. Mech Dev 113:141–148PubMedGoogle Scholar
  204. Inoue Y, Niwa N, Mito T, Ohuchi H, Yoshioka H, Noji S (2002b) Expression patterns of hedgehog, wingless, and decapentaplegic during gut formation of Gryllus bimaculatus (cricket). Mech Dev 110:245–248PubMedGoogle Scholar
  205. 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 4:725–731PubMedGoogle Scholar
  206. Jaeger J (2011) The gap gene network. Cell Mol Life Sci 68:243–274PubMedCentralPubMedGoogle Scholar
  207. Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 23:125–133PubMedGoogle Scholar
  208. Jang CC, Chao JL, Jones N, Yao LC, Bessarab DA, Kuo YM, Jun S, Desplan C, Beckendorf SK, Sun YH (2003) Two Pax genes, eye gone and eyeless, act cooperatively in promoting Drosophila eye development. Development 130:2939–2951PubMedGoogle Scholar
  209. Janssen R (2013) Developmental abnormalities in Glomeris marginata (Villers 1789) (Myriapoda: Diplopoda): implications for body axis determination in a myriapod. Naturwissenschaften 100:33–43PubMedGoogle Scholar
  210. Janssen R, Damen WG (2008) Diverged and conserved aspects of heart formation in a spider. Evol Dev 10:155–165PubMedGoogle Scholar
  211. Janssen R, Eriksson BJ, Budd GE, Akam M, Prpic N-M (2010) Gene expression patterns in an onychophoran reveal that regionalization predates limb segmentation in pan-arthropods. Evol Dev 12:363–372PubMedGoogle Scholar
  212. Janssen R, Eriksson BJ, Tait NN, Budd GE (2014) Onychophoran Hox genes and the evolution of arthropod Hox gene expression. Front Zool 11:22PubMedCentralPubMedGoogle Scholar
  213. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137:1343–1355PubMedCentralPubMedGoogle Scholar
  214. Jockusch EL, Nagy LM (1997) Insect evolution: how did insect wings originate? Curr Biol 7:R358–R361PubMedGoogle Scholar
  215. Jockusch EL, Ober KA (2004) Hypothesis testing in evolutionary developmental biology: a case study from insect wings. J Hered 95:382–396PubMedGoogle Scholar
  216. Jockusch EL, Nulsen C, Newfeld SJ, Nagy LM (2000) Leg development in flies versus grasshoppers: differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development 127:1617–1626PubMedGoogle Scholar
  217. Jockusch EL, Williams TA, Nagy LM (2004) The evolution of patterning of serially homologous appendages in insects. Dev Genes Evol 214:324–338PubMedGoogle Scholar
  218. Johnston LA, Schubiger G (1996) Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination. Development 122:3519–3529PubMedGoogle Scholar
  219. Jory A, Estella C, Giorgianni MW, Slattery M, Laverty TR, Rubin GM, Mann RS (2012) A survey of 6,300 genomic fragments for cis-regulatory activity in the imaginal discs of Drosophila melanogaster. Cell Rep 2:1014–1024PubMedCentralPubMedGoogle Scholar
  220. Kainz F, Ewen-Campen B, Akam M, Extavour CG (2011) Notch/Delta signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus. Development 138:5015–5026PubMedGoogle Scholar
  221. Kaufman TC, Lewis R, Wakimoto B (1980) Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: the homoeotic gene complex in polytene chromosome interval 84a-B. Genetics 94:115–133PubMedCentralPubMedGoogle Scholar
  222. Kawakami Y, Esteban CR, Raya M, Kawakami H, Marti M, Dubova I, Belmonte JCI (2006) Wnt/β-catenin signaling regulates vertebrate limb regeneration. Genes Dev 20:3232–3237PubMedCentralPubMedGoogle Scholar
  223. Kelsh R, Dawson I, Akam M (1993) An analysis of Abdominal-B expression in the locust Schistocerca gregaria. Development 117:293–305PubMedGoogle Scholar
  224. Kerber B, Monge I, Mueller M, Mitchell PJ, Cohen SM (2001) The AP-2 transcription factor is required for joint formation and cell survival in Drosophila leg development. Development 128:1231–1238PubMedGoogle Scholar
  225. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532–534PubMedGoogle Scholar
  226. Khila A, Abouheif E (2008) Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Proc Natl Acad Sci U S A 105:17884–17889PubMedCentralPubMedGoogle Scholar
  227. Khila A, Abouheif E, Rowe L (2009) Evolution of a novel appendage ground plan in water striders is driven by changes in the Hox gene Ultrabithorax. PLoS Genet 5:e1000583PubMedCentralPubMedGoogle Scholar
  228. Khila A, Abouheif E, Rowe L (2012) Function, developmental genetics, and fitness consequences of a sexually antagonistic trait. Science 336:585–589PubMedGoogle Scholar
  229. Khila A, Abouheif E, Rowe L (2014) Comparative functional analyses of Ultrabithorax reveal multiple steps and paths to diversification of legs in the adaptive radiation of semi-aquatic insects. Evolution 68:2159–2170PubMedGoogle Scholar
  230. Kijimoto T, Moczek AP, Andrews J (2012) Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc Natl Acad Sci U S A 109:20526–20531PubMedCentralPubMedGoogle Scholar
  231. Kim CW (1959) The differentiation centre inducing the development from larval to adult leg in Pieris brassicae (Lepidoptera). J Embryol Exp Morphol 7:572–582PubMedGoogle Scholar
  232. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A (1997) Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388:304–308PubMedGoogle Scholar
  233. Kingsolver JG (1995) Viability selection on seasonally polyphenic traits: wing melanin pattern in western white butterflies. Evolution 49:932–941Google Scholar
  234. Klag J, Swiatek P (1999) Differentiation of primordial germ cells during embryogenesis of Allacma fusca (L.) (Collembola: Symphypleona). Int J Insect Morphol Embryol 28:161–168Google Scholar
  235. Klebes A, Biehs B, Cifuentes F, Kornberg TB (2002) Expression profiling of Drosophila imaginal discs. Genome Biol 3:0038.1–0038.16Google Scholar
  236. Klebes A, Sustar A, Kechris K, Li H, Schubiger G, Kornberg TB (2005) Regulation of cellular plasticity in Drosophila imaginal disc cells by the Polycomb group, trithorax group and lama genes. Development 132:3753–3765PubMedGoogle Scholar
  237. Knüttel H, Fiedler K (2001) Host-plant-derived variation in ultraviolet wing patterns influences mate selection by male butterflies. J Exp Biol 204:2447–2459PubMedGoogle Scholar
  238. Koch PB, Behnecke B, french-Constant RH (2000) The molecular basis of melanism and mimicry in a swallowtail butterfly. Curr Biol 10:591–594Google Scholar
  239. Kojima T, Tsuji T, Saigo K (2005) A concerted action of a paired-type homeobox gene, aristaless, and a homolog of Hox11/tlx homeobox gene, clawless, is essential for the distal tip development of the Drosophila leg. Dev Biol 279:434–445PubMedGoogle Scholar
  240. Konopova B, Akam M (2014) The Hox genes Ultrabithorax and abdominal-A specify three different types of abdominal appendage in the springtail Orchesella cincta (Collembola). EvoDevo 5:2PubMedCentralPubMedGoogle Scholar
  241. Kragl M, Knapp D, Nacu E, Khattak S, Maden M, Epperlein HH, Tanaka EM (2009) Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460:60–65PubMedGoogle Scholar
  242. Kukalová-Peck J (1983) Origin of the insect wing and wing articulation from the arthropodan leg. Can J Zool 61:1618–1669Google Scholar
  243. Kukalová-Peck J (1992) The “Uniramia” do not exist: the ground plan of the Pterygota as revealed by Permian Diaphanopterodea from Russia (Insecta: Paleodictyopteroidea). Can J Zool 70:236–255Google Scholar
  244. Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR (2014) doublesex is a mimicry supergene. Nature 507:229–232PubMedGoogle Scholar
  245. Kux K, Kiparaki M, Delidakis C (2013) The two Tribolium E(spl) genes show evolutionarily conserved expression and function during embryonic neurogenesis. Mech Dev 130:207–225PubMedGoogle Scholar
  246. Lall S, Ludwig MZ, Patel NH (2003) Nanos plays a conserved role in axial patterning outside of the Diptera. Curr Biol 13:224–229PubMedGoogle Scholar
  247. Land MF, Nilsson DE (2012) In: Willmer P, Norman D (eds) Animal eyes. Oxford University Press, OxfordGoogle Scholar
  248. Lawrence PA, Morata G (1977) The early development of mesothoracic compartments in Drosophila. An analysis of cell lineage and fate mapping and an assessment of methods. Dev Biol 56:40–51PubMedGoogle Scholar
  249. Lebreton G, Faucher C, Cribbs DL, Benassayag C (2008) Timing of Wingless signalling distinguishes maxillary and antennal identities in Drosophila melanogaster. Development 135:2301–2309Google Scholar
  250. Lecuit T, Cohen SM (1997) Proximal – distal axis formation in the Drosophila leg. Nature 388:139–145PubMedGoogle Scholar
  251. Lecuit T, Brook WJ, Ng M, Calleja M, Sun H, Cohen SM (1996) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381:387–393PubMedGoogle Scholar
  252. 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
  253. Lee AK, Sze CC, Kim ER, Suzuki Y (2013) Developmental coupling of larval and adult stages in a complex life cycle: insights from limb regeneration in the flour beetle, Tribolium castaneum. EvoDevo 4:20PubMedCentralPubMedGoogle Scholar
  254. Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Ozbek S, Bode H, Holstein TW (2009) Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 330:186–199PubMedGoogle Scholar
  255. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570PubMedGoogle Scholar
  256. Lewis DL, DeCamillis M, Bennett RL (2000) Distinct roles of the homeotic genes Ubx and abd-A in beetle embryonic abdominal appendage development. Proc Natl Acad Sci 97:4504–4509PubMedCentralPubMedGoogle Scholar
  257. Li H, Popadić A (2004) Analysis of nubbin expression patterns in insects. Evol Dev 6:310–324PubMedGoogle Scholar
  258. Lin G-W, Cook CE, Miura T, Chang C-C (2014a) Posterior localization of ApVas1 positions the preformed germ plasm in the sexual oviparous pea aphid Acyrthosiphon pisum. EvoDevo 5:18PubMedCentralPubMedGoogle Scholar
  259. Lin X, Yao Y, Jin M, Li Q (2014b) Characterization of the Distal-less gene homologue, NlDll, in the brown planthopper, Nilaparvata lugens (Stål). Gene 535:112–118PubMedGoogle Scholar
  260. Liubicich DM, Serano JM, Pavlopoulos A, Kontarakis Z, Protas ME, Kwan E, Chatterjee S, Tran KD, Averof M, Patel NH (2009) Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc Natl Acad Sci 106:13892–13896PubMedCentralPubMedGoogle Scholar
  261. Loehlin DW, Werren JH (2012) Evolution of shape by multiple regulatory changes to a growth gene. Science 335:943–947PubMedCentralPubMedGoogle Scholar
  262. Loehlin DW, Oliveira DCSG, Edwards R, Giebel JD, Clark ME, Cattani MV, van de Zande L, Verhulst EC, Beukeboom LW, Muñoz-Torres M, Werren JH (2010) Non-coding changes cause sex-specific wing size differences between closely related species of Nasonia. PLoS Genet 6:e1000821PubMedCentralPubMedGoogle Scholar
  263. Lopes CS, Casares F (2010) hth maintains the pool of eye progenitors and its downregulation by Dpp and Hh couples retinal fate acquisition with cell cycle exit. Dev Biol 339:78–88PubMedGoogle Scholar
  264. Lynch JA, Desplan C (2010) Novel modes of localization and function of nanos in the wasp Nasonia. Development 137:3813–3821PubMedCentralPubMedGoogle Scholar
  265. Lynch JA, Özüak O, Khila A, Abouheif E, Desplan C, Roth S (2011) The phylogenetic origin of oskar coincided with the origin of maternally provisioned germ plasm and pole cells at the base of the Holometabola. PLoS Genet 7:e1002029PubMedCentralPubMedGoogle Scholar
  266. Lyytinen A, Brakefield PM, Lindstrom L, Mappes J (2004) Does predation maintain eyespot plasticity in Bicyclus anynana? Proc R Soc B Biol Sci 271:279–283Google Scholar
  267. Ma C, 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 75:927–938PubMedGoogle Scholar
  268. Macdonald WP, Martin A, Reed RD (2010) Butterfly wings shaped by a molecular cookie cutter: evolutionary radiation of lepidopteran wing shapes associated with a derived Cut/wingless wing margin boundary system. Evol Dev 12:296–304PubMedGoogle Scholar
  269. Machida R (1981) External features of embryonic development of a jumping bristletail, Pedetontus unimaculatus Machida (Insecta, Thysanura, Machilidae). J Morphol 168:339–355Google Scholar
  270. Machida R (2000) Serial homology of the mandible and maxilla in the jumping bristletail Pedetontus unimaculatus Machida, based on external embryology (Hexapoda: Archaeognatha, Machilidae). J Morphol 245:19–28PubMedGoogle Scholar
  271. 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 101:4877–4882PubMedCentralPubMedGoogle Scholar
  272. Mahfooz N, Turchyn N, Mihajlovic M, Hrycaj S, Popadić A (2007) Ubx regulates differential enlargement and diversification of insect hind legs. PLoS One 2:e866PubMedCentralPubMedGoogle Scholar
  273. Mahowald AP (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203:187–213PubMedGoogle Scholar
  274. Manjón C, Sánchez-Herrero E, Suzanne M (2007) Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9:57–63PubMedGoogle Scholar
  275. Manton SM (1964) Mandibular mechanisms and the evolution of arthropods. Phil Trans R Soc B 247:1–183Google Scholar
  276. Mardon G, Solomon NM, Rubin GM (1994) dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120:3473–3486PubMedGoogle Scholar
  277. Martin A, Reed RD (2010) wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution. Mol Biol Evol 27:2864–2878PubMedGoogle Scholar
  278. Martin A, Reed RD (2014) Wnt signaling underlies evolution and development of the butterfly wing pattern symmetry systems. Dev Biol 395:367–378PubMedGoogle Scholar
  279. Martin A, McCulloch KJ, Patel NH, Briscoe AD, Gilbert LE, Reed RD (2014) Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations. EvoDevo 5:1–14Google Scholar
  280. Maruzzo D, Bortolin F (2013) Arthropod regeneration. In: Minelli A, Boxshall G, Fusco G (eds) Arthropod biology and evolution: molecules, development, morphology. Springer, HeidelbergGoogle Scholar
  281. Masucci JD, Miltenberger RJ, Hoffmann FM (1990) Pattern-specific expression of the Drosophila decapentaplegic gene in imaginal disks is regulated by 3′ cis-regulatory elements. Genes Dev 4:2011–2023PubMedGoogle Scholar
  282. Masumoto M, Yaginuma T, Niimi T (2009) Functional analysis of Ultrabithorax in the silkworm, Bombyx mori, using RNAi. Dev Genes Evol 219:437–444PubMedGoogle Scholar
  283. Matsuda S, Shimmi O (2012) Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila. Dev Biol 366:153–162PubMedGoogle Scholar
  284. Matsuda S, Yoshiyama N, Künnapuu-Vulli J, Hatakeyama M, Shimmi O (2013) Dpp/BMP transport mechanism is required for wing venation in the sawfly Athalia rosae. Insect Biochem Mol Biol 43:466–473PubMedGoogle Scholar
  285. Maurel-Zaffran C, Treisman JE (2000) pannier acts upstream of wingless to direct dorsal eye disc development in Drosophila. Development 127:1007–1016PubMedGoogle Scholar
  286. Maves L, Schubiger G (1998) A molecular basis for transdetermination in Drosophila imaginal discs: interactions between wingless and decapentaplegic signaling. Development 125:115–124PubMedGoogle Scholar
  287. McClure KD, Schubiger G (2005) Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132:5033–5042PubMedGoogle Scholar
  288. McClure KD, Sustar A, Schubiger G (2008) Three genes control the timing, the site and the size of blastema formation in Drosophila. Dev Biol 319:68–77PubMedCentralPubMedGoogle Scholar
  289. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302PubMedGoogle Scholar
  290. McGinnis N, Ragnhildstveit E, Veraksa A, McGinnis W (1998) A cap‘n’collar protein isoform contains a selective Hox repressor function. Development 125:4553–4564Google Scholar
  291. McKay DJ, Lieb JD (2013) A common set of DNA regulatory elements shapes Drosophila appendages. Dev Cell 27:306–318PubMedGoogle Scholar
  292. McKay DJ, Estella C, Mann RS (2009) The origins of the Drosophila leg revealed by the cis-regulatory architecture of the Distalless gene. Development 136:61–71PubMedCentralPubMedGoogle Scholar
  293. McNeill H, Yang CH, Brodsky M, Ungos J, Simon MA (1997) mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev 11:1073–1082PubMedGoogle Scholar
  294. Medved V, Huang ZY, Popadic A (2014) Ubx promotes corbicular development in Apis mellifera. Biol Lett 10:20131021PubMedCentralPubMedGoogle Scholar
  295. Meinhardt H (1983) Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol 96:375–385PubMedGoogle Scholar
  296. Merrill VK, Turner FR, Kaufman TC (1987) A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster. Dev Biol 122:379–395PubMedGoogle Scholar
  297. Mirth C, Akam M (2002) Joint development in the Drosophila leg: cell movements and cell populations. Dev Biol 246:391–406PubMedGoogle Scholar
  298. Mito T, Inoue Y, Kimura S, Miyawaki K, Niwa N, Shinmyo Y, Ohuchi H, Noji S (2002) Involvement of hedgehog, wingless, and dpp in the initiation of proximodistal axis formation during the regeneration of insect legs, a verification of the modified boundary model. Mech Dev 114:27–35PubMedGoogle Scholar
  299. Mito T, Ronco M, Uda T, Nakamura T, Ohuchi H, Noji S (2008) Divergent and conserved roles of extradenticle in body segmentation and appendage formation, respectively, in the cricket Gryllus bimaculatus. Dev Biol 313:67–79PubMedGoogle Scholar
  300. Mito T, Shinmyo Y, Kurita K, Nakamura T, Ohuchi H, Noji S (2011) Ancestral functions of Delta/Notch signaling in the formation of body and leg segments in the cricket Gryllus bimaculatus. Development 138:3823–3833PubMedGoogle Scholar
  301. Mitten EK, Jing D, Suzuki Y (2012) Matrix metalloproteinases (MMPs) are required for wound closure and healing during larval leg regeneration in the flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 42:854–864PubMedGoogle Scholar
  302. Mittmann B, Scholtz G (2001) Distal-less expression in embryos of Limulus polyphemus (Chelicerata, Xiphosura) and Lepisma saccharina (Insecta, Zygentoma) suggests a role in the development of mechanoreceptors, chemoreceptors, and the CNS. Dev Genes Evol 211:232–243PubMedGoogle Scholar
  303. Miyawaki K, Inoue Y, Mito T, Fujimoto T, Matsushima K, Shinmyo Y, Ohuchi H, Noji S (2002) Expression patterns of aristaless in developing appendages of Gryllus bimaculatus (cricket). Mech Dev 113:181–184PubMedGoogle Scholar
  304. Miyawaki K, Mito T, Sarashina I, Zhang H, Shinmyo Y, Ohuchi H, Noji S (2004) Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech Dev 121:119–130PubMedGoogle Scholar
  305. Mlodzik M, Fjose A, Gehring WJ (1988) Molecular structure and spatial expression of a homeobox gene from the labial region of the Antennapedia-complex. EMBO J 7:2569–2578PubMedCentralPubMedGoogle Scholar
  306. Moczek AP, Nagy LM (2005) Diverse developmental mechanisms contribute to different levels of diversity in horned beetles. Evol Dev 7:175–185PubMedGoogle Scholar
  307. Moczek AP, Rose DJ (2009) Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proc Natl Acad Sci 106:8992–8997PubMedCentralPubMedGoogle Scholar
  308. Mohler J (1993) Genetic regulation of CNC expression in the pharyngeal primordia of Drosophila blastoderm embryos. Roux’s Arch Dev Biol 202:214–223Google Scholar
  309. Montagne J, Groppe J, Guillemin K, Krasnow MA, Gehring WJ, Affolter M (1996) The Drosophila Serum Response Factor gene is required for the formation of intervein tissue of the wing and is allelic to blistered. Development 122:2589–2597PubMedGoogle Scholar
  310. Monteiro A, Chen B, Ramos DM, Oliver JC, Tong X, Guo M, WANG W-K, Fazzino L, Kamal F (2013) Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J Exp Zool B Mol Dev Evol 320:321–331PubMedGoogle Scholar
  311. Nagata T, Suzuki Y, Ueno K, Kokubo H, Xu X, Hui C, Hara W, Fukuta M (1996) Developmental of the Bombyx Antennapedia homologue and homeotic changes in the Nc mutant. Genes Cells 1:555–568PubMedGoogle Scholar
  312. Nakamura T, Mito T, Tanaka Y, Bando T, Ohuchi H, Noji S (2007) Involvement of canonical Wnt/Wingless signaling in the determination of the positional values within the leg segment of the cricket Gryllus bimaculatus: wnt signaling in cricket leg regeneration. Dev Growth Differ 49:79–88Google Scholar
  313. Nakamura T, Mito T, Bando T, Ohuchi H, Noji S (2008a) Dissecting insect leg regeneration through RNA interference. Cell Mol Life Sci 65:64–72PubMedGoogle Scholar
  314. Nakamura T, Mito T, Miyawaki K, Ohuchi H, Noji S (2008b) EGFR signaling is required for re-establishing the proximodistal axis during distal leg regeneration in the cricket Gryllus bimaculatus nymph. Dev Biol 319:46–55PubMedGoogle Scholar
  315. Nakao H (1999) Isolation and characterization of a Bombyx vasa-like gene. Dev Genes Evol 209:312–316PubMedGoogle Scholar
  316. Nakao H, Hatakeyama M, Lee JM, Shimoda M, Kanda T (2006) Expression pattern of Bombyx vasa-like (BmVLG) protein and its implications in germ cell development. Dev Genes Evol 216:94–99PubMedGoogle Scholar
  317. Nakao H, Matsumoto T, Oba Y, Niimi T, Yaginuma T (2008) Germ cell specification and early embryonic patterning in Bombyx mori as revealed by nanos orthologues. Evol Dev 10:546–554PubMedGoogle Scholar
  318. Namigai EKO, Suzuki Y (2012) Functional conservation and divergence of BMP ligands in limb development and lipid homeostasis of holometabolous insects. Evol Dev 14:296–310PubMedGoogle Scholar
  319. Natori K, Tajiri R, Furukawa S, Kojima T (2012) Progressive tarsal patterning in the Drosophila by temporally dynamic regulation of transcription factor genes. Dev Biol 361:450–462PubMedGoogle Scholar
  320. Negre B, Ruiz A (2007) HOM-C evolution in Drosophila: is there a need for Hox gene clustering? Trends Genet 23:55–59PubMedGoogle Scholar
  321. Nellen D, Burke R, Struhl G, Basler K (1996) Direct and long-range action of a DPP morphogen gradient. Cell 85:357–368PubMedGoogle Scholar
  322. Neumann CJ, Cohen SM (1996) A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing. Development 122:3477–3485PubMedGoogle Scholar
  323. Neumann CJ, Cohen SM (1997) Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124:871–880PubMedGoogle Scholar
  324. Ng M, Diaz-Benjumea FJ, Cohen SM (1995) nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development 121:589–599PubMedGoogle Scholar
  325. Nicholson DB, Ross AJ, Mayhew PJ (2014) Fossil evidence for key innovations in the evolution of insect diversity. Proc R Soc B: Biol Sci 281:20141823Google Scholar
  326. Niimi T, Kuwayama H, Yaginuma T (2005) Larval RNAi applied to the analysis of postembryonic development in the ladybird beetle, Harmonia axyridis. J Insect Biotechnol Sericology 74:95–102Google Scholar
  327. Nijhout HF (1980) Pattern formation on lepidopteran wings: determination of an eyespot. Dev Biol 80:267–274PubMedGoogle Scholar
  328. Nijhout HF (1991) The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, DCGoogle Scholar
  329. Nijhout HF (1994) Symmetry systems and compartments in Lepidopteran wings: the evolution of a patterning mechanism. Development 1994:225–233Google Scholar
  330. Niwa N, Saito M, Ohuchi H, Yoshioka H, Noji S (1997) Correlation between Distal-less expression patterns and structures of appendages in development of the two-spotted cricket, Gryllus bimaculatus. Zool Sci 14:115–125Google Scholar
  331. 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
  332. Niwa N, Akimoto-Kato A, Niimi T, Tojo K, Machida R, Hayashi S (2010) Evolutionary origin of the insect wing via integration of two developmental modules: new hypothesis of insect wing evolution. Evol Dev 12:168–176PubMedGoogle Scholar
  333. Ober KA, Jockusch EL (2006) The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol 294:391–405PubMedGoogle Scholar
  334. Ohde T, Masumoto M, Morita-Miwa M, Matsuura H, Yoshioka H, Yaginuma T, Niimi T (2009a) Vestigial and scalloped in the ladybird beetle: a conserved function in wing development and a novel function in pupal ecdysis. Insect Mol Biol 18:571–581PubMedGoogle Scholar
  335. Ohde T, Masumoto M, Yaginuma T, Niimi T (2009b) Embryonic RNAi analysis in the firebrat, Thermobia domestica (Zygentoma: Lepismatidae): Distal-less is required to form caudal filament. J Insect Biotechnol Sericology 78:99–105Google Scholar
  336. Ohde T, Yaginuma T, Niimi T (2011) Nymphal RNAi analysis reveals novel function of scalloped in antenna, cercus and caudal filament formation in the firebrat, Thermobia domestica. J Insect Biotechnol Sericology 80(3):101–108Google Scholar
  337. Ohde T, Yaginuma T, Niimi T (2013) Insect morphological diversification through the modification of wing serial homologs. Science 340:495–498PubMedGoogle Scholar
  338. Oka K, Yoshiyama N, Tojo K, Machida R, Hatakeyama M (2010) Characterization of abdominal appendages in the sawfly, Athalia rosae (Hymenoptera), by morphological and gene expression analyses. Dev Genes Evol 220:53–59PubMedGoogle Scholar
  339. Olesen J, Richter S, Scholtz G (2001) The evolutionary transformation of phyllopodous to stenopodous limbs in the Branchiopoda (Crustacea)-is there a common mechanism for early limb development in arthropods? Int J Dev Biol 45:869–876PubMedGoogle Scholar
  340. Oliver JC, Tong X-L, Gall LF, Piel WH, Monteiro A (2012) A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet 8:e1002893PubMedCentralPubMedGoogle Scholar
  341. Page-McCaw A, Serano J, Sante JM, Rubin GM (2003) Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development. Dev Cell 4:95–106PubMedGoogle Scholar
  342. Palopoli MF, Patel NH (1998) Evolution of the interaction between Hox genes and a downstream target. Curr Biol 8:587–590PubMedGoogle Scholar
  343. Panganiban G, Nagy L, Carroll SB (1994) The role of the Distal-less gene in the development and evolution of insect limbs. Curr Biol 4:671–675PubMedGoogle Scholar
  344. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363–1366PubMedGoogle Scholar
  345. Papa R, Martin A, Reed RD (2008) Genomic hotspots of adaptation in butterfly wing pattern evolution. Curr Opin Genet Dev 18:559–564PubMedGoogle Scholar
  346. Papayannopoulos V, Tomlinson A, Panin VM, Rauskolb C, Irvine KD (1998) Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034PubMedGoogle Scholar
  347. Pappu KS, Mardon G (2004) Genetic control of retinal specification and determination in Drosophila. Int J Dev Biol 48:913–924PubMedGoogle Scholar
  348. Passalacqua KD, Hrycaj S, Mahfooz N, Popadić A (2010) Evolving expression patterns of the homeotic gene Scr in insects. Int J Dev Biol 54:897–904PubMedGoogle Scholar
  349. Pattatucci AM, Otteson DC, Kaufman TC (1991) A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster. Genetics 129:423–441PubMedCentralPubMedGoogle Scholar
  350. Paul L, Wang S-H, Manivannan SN, Bonanno L, Lewis S, Austin CL, Simcox A (2013) Dpp-induced Egfr signaling triggers postembryonic wing development in Drosophila. Proc Natl Acad Sci 110:5058–5063PubMedCentralPubMedGoogle Scholar
  351. Paulus H (2000) Phylogeny of the Myriapoda–Crustacea–Insecta: a new attempt using photoreceptor structure. J Zool Syst Evol Res 38:189–208Google Scholar
  352. Pavlopoulos A, Akam M (2011) Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis. Proc Natl Acad Sci 108:2855–2860PubMedCentralPubMedGoogle Scholar
  353. Pavlopoulos A, Kontarakis Z, Liubicich DM, Serano JM, Akam M, Patel NH, Averof M (2009) Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean. Proc Natl Acad Sci 106:13897–13902PubMedCentralPubMedGoogle Scholar
  354. Peel AD, Chipman AD, Akam M (2005) Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6:905–916PubMedGoogle Scholar
  355. Petersen CP, Reddien PW (2008) Smed-βcatenin-1 is required for anteroposterior blastema polarity in planarian regeneration. Science 319:327–330Google Scholar
  356. Peterson MD, Rogers BT, Popadić A, Kaufman TC (1999) The embryonic expression pattern of labial, homeotic complex genes and the teashirt homologue in an apterygote insect. Dev Genes Evol 209:77–90PubMedGoogle Scholar
  357. Pignoni F, Zipursky SL (1997) Induction of Drosophila eye development by decapentaplegic. Development 124:271–278PubMedGoogle Scholar
  358. Pignoni F, Hu B, Zavitz KH, Xiao J, Garrity PA, Zipursky SL (1997) The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development. Cell 91:881–891PubMedGoogle Scholar
  359. Popadić A, Panganiban G, Rusch D, Shear WA, Kaufman TC (1998) Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev Genes Evol 208:142–150PubMedGoogle Scholar
  360. Posnien N, Bucher G (2010) Formation of the insect head involves lateral contribution of the intercalary segment, which depends on Tc-labial function. Dev Biol 338:107–116PubMedGoogle Scholar
  361. Posnien N, Bashasab F, Bucher G (2009) The insect upper lip (labrum) is a nonsegmental appendage-like structure. Evol Dev 11:480–488PubMedGoogle Scholar
  362. Prpic NM, Damen WG (2004) Expression patterns of leg genes in the mouthparts of the spider Cupiennius salei (Chelicerata: Arachnida). Dev Genes Evol 214:296–302PubMedGoogle Scholar
  363. Prpic N-M, Damen WGM (2009) Notch-mediated segmentation of the appendages is a molecular phylotypic trait of the arthropods. Dev Biol 326:262–271PubMedGoogle Scholar
  364. Prpic N-M, Tautz D (2003) The expression of the proximodistal axis patterning genes Distal-less and dachshund in the appendages of Glomeris marginata (Myriapoda: Diplopoda) suggests a special role of these genes in patterning the head appendages. Dev Biol 260:97–112PubMedGoogle Scholar
  365. Prpic N-M, Wigand B, Damen W, Klingler M (2001) Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol 211:467–477PubMedGoogle Scholar
  366. Prpic N-M, Janssen R, Wigand B, Klingler M, Damen WG (2003) Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling. Dev Biol 264:119–140PubMedGoogle Scholar
  367. Prud’homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh S-D, True JR, Carroll SB (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440:1050–1053PubMedGoogle Scholar
  368. Pueyo JI, Couso JP (2008) The 11-aminoacid long Tarsal-less peptides trigger a cell signal in Drosophila leg development. Dev Biol 324:192–201PubMedGoogle Scholar
  369. Pueyo JI, Couso JP (2011) Tarsal-less peptides control Notch signalling through the Shavenbaby transcription factor. Dev Biol 355:183–193PubMedCentralPubMedGoogle Scholar
  370. Pueyo JI, Lanfear R, Couso JP (2008) Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana. Proc Natl Acad Sci 105:16614–16619PubMedCentralPubMedGoogle Scholar
  371. Pultz MA, Diederich RJ, Cribbs DL, Kaufman TC (1988) The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis. Genes Dev 2:901–920PubMedGoogle Scholar
  372. Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and aniridia in humans. Science 265:785–789PubMedGoogle Scholar
  373. Rauskolb C (2001) The establishment of segmentation in the Drosophila leg. Development 128:4511–4521PubMedGoogle Scholar
  374. Rauskolb C, Irvine KD (1999) Notch-mediated segmentation and growth control of the Drosophila leg. Dev Biol 210:339–350PubMedGoogle Scholar
  375. Reed RD (2004) Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales. Dev Genes Evol 214:43–46PubMedGoogle Scholar
  376. Reed RD, Nagy LM (2005) Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evol Dev 7:301–311PubMedGoogle Scholar
  377. Reed RD, Serfas MS (2004) Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr Biol 14:1159–1166PubMedGoogle Scholar
  378. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO (2011) optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–1141PubMedGoogle Scholar
  379. Refki NP, Armisén D, Crumière AJJ, Viala S, Khila A (2014) Emergence of tissue sensitivity to Hox protein levels underlies the evolution of an adaptive morphological trait. Dev Biol 392:441–453PubMedCentralPubMedGoogle Scholar
  380. Regulski M, Harding K, Kostriken R, Karch F, Levine M, McGinnis W (1985) Homeo box genes of the Antennapedia and Bithorax complexes of Drosophila. Cell 43:71–80PubMedGoogle Scholar
  381. Regulski M, McGinnis N, Chadwick R, McGinnis W (1987) Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development. EMBO J 6:767–777PubMedCentralPubMedGoogle Scholar
  382. Reifegerste R, Moses K (1999) Genetics of epithelial polarity and pattern in the Drosophila retina. Bioessays 21:275–285PubMedGoogle Scholar
  383. Restrepo S, Zartman JJ, Basler K (2014) Coordination of patterning and growth by the morphogen DPP. Curr Biol 24:R245–R255PubMedGoogle Scholar
  384. Riek EF, Kukalová-Peck J (1984) A new interpretation of dragonfly wing venation based upon early upper Carboniferous fossils from Argentina (Insecta: Odonatoidea) and basic character states in pterygote wings. Can J Zool 62:1150–1166Google Scholar
  385. Rogers BT, Peterson MD, Kaufman TC (1997) Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. Development 124:149–157PubMedGoogle Scholar
  386. Rogers BT, Peterson MD, Kaufman TC (2002) The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol Dev 4:96–110PubMedGoogle Scholar
  387. Ronco M, Uda T, Mito T, Minelli A, Noji S, Klingler M (2008) Antenna and all gnathal appendages are similarly transformed by homothorax knock-down in the cricket Gryllus bimaculatus. Dev Biol 313:80–92PubMedGoogle Scholar
  388. Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917PubMedGoogle Scholar
  389. Rost MM, Flakus A, Klag J (2005) Primordial germ cell differentiation in natural and manipulated twin embryos of Thermobia domestica (Insecta: Zygentoma). Ann Entomol Soc Am 98:108–112Google Scholar
  390. Saenko SV, Marialva MS, Beldade P (2011) Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2:9PubMedCentralPubMedGoogle Scholar
  391. Sanchez-Salazar J, Pletcher MT, Bennett RL, Brown SJ, Dandamudi TJ, Denell RE, Doctor JS (1996) The Tribolium decapentaplegic gene is similar in sequence, structure, and expression to the Drosophila dpp gene. Dev Genes Evol 206:237–246PubMedGoogle Scholar
  392. Santos AC, Lehmann R (2004) Germ cell specification and migration in Drosophila and beyond. Curr Biol 14:R578–R589PubMedGoogle Scholar
  393. Sato K, Matsunaga TM, Futahashi R, Kojima T, Mita K, Banno Y, Fujiwara H (2008) Positional cloning of a Bombyx wingless locus flügellos (fl) reveals a crucial role for fringe that is specific for wing morphogenesis. Genetics 179:875–885PubMedCentralPubMedGoogle Scholar
  394. Savard J, Marques-Souza H, Aranda M, Tautz D (2006) A segmentation gene in Tribolium produces a polycistronic mRNA that codes for multiple conserved peptides. Cell 126:559–569PubMedGoogle Scholar
  395. Schaeper ND, Wimmer EA, Prpic N-M (2013) Appendage patterning in the primitively wingless hexapods Thermobia domestica (Zygentoma: Lepismatidae) and Folsomia candida (Collembola: Isotomidae). Dev Genes Evol 223:341–350PubMedGoogle Scholar
  396. Schinko JB, Kreuzer N, Offen N, Posnien N, Wimmer EA, Bucher G (2008) Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Dev Biol 317:600–613PubMedGoogle Scholar
  397. Schmitt-Engel C, Cerny AC, Schoppmeier M (2012) A dual role for nanos and pumilio in anterior and posterior blastodermal patterning of the short-germ beetle Tribolium castaneum. Dev Biol 364:224–235PubMedGoogle Scholar
  398. Schnellhammer I (2012) Evolution früher Faktoren der Segmentierungskaskade: Funktionelle Untersuchungen in Bruchidius, Tribolium und Oncopeltus. Ph.D. Dissertation, Friedrich-Alexander Universität Erlangen-NürnbergGoogle Scholar
  399. Scholtz G, Mittmann B, Gerberding M (1998) The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42:801–810PubMedGoogle Scholar
  400. Schröder R (2006) vasa mRNA accumulates at the posterior pole during blastoderm formation in the flour beetle Tribolium castaneum. Dev Genes Evol 216:277–283PubMedGoogle Scholar
  401. Schubiger M, Sustar A, Schubiger G (2010) Regeneration and transdetermination: the role of wingless and its regulation. Dev Biol 347:315–324PubMedCentralPubMedGoogle Scholar
  402. Sewell W, Williams T, Cooley J, Terry M, Ho R, Nagy L (2008) Evidence for a novel role for dachshund in patterning the proximal arthropod leg. Dev Genes Evol 218:293–305PubMedGoogle Scholar
  403. Shah MV, Namigai EK, Suzuki Y (2011) The role of canonical Wnt signaling in leg regeneration and metamorphosis in the red flour beetle Tribolium castaneum. Mech Dev 128:342–358PubMedGoogle Scholar
  404. Sharma PP, Schwager EE, Extavour CG, Giribet G (2012) Evolution of the chelicera: a dachshund domain is retained in the deutocerebral appendage of Opiliones (Arthropoda, Chelicerata). Evol Dev 14:522–533PubMedGoogle Scholar
  405. Sharma PP, Schwager EE, Giribet G, Jockusch EL, Extavour CG (2013) Distal-less and dachshund pattern both plesiomorphic and apomorphic structures in chelicerates: RNA interference in the harvestman Phalangium opilio (Opiliones). Evol Dev 15:228–242PubMedGoogle Scholar
  406. Sharma PP, Gupta T, Schwager EE, Wheeler WC, Extavour CG (2014) Subdivision of arthropod cap-n-collar expression domains is restricted to Mandibulata. EvoDevo 5:3PubMedCentralPubMedGoogle Scholar
  407. Shbailat SJ, Abouheif E (2013) The wing-patterning network in the wingless castes of myrmicine and formicine species is a mix of evolutionarily labile and non-labile genes. J Exp Zool B Mol Dev Evol 320B:74–83Google Scholar
  408. Shbailat SJ, Khila A, Abouheif E (2010) Correlations between spatiotemporal changes in gene expression and apoptosis underlie wing polyphenism in the ant Pheidole morrisi: network architecture underlying polyphenism. Evol Dev 12:580–591PubMedGoogle Scholar
  409. Shimmi O, Matsuda S, Hatakeyama M (2014) Insights into the molecular mechanisms underlying diversified wing venation among insects. Proc R Soc B: Biol Sci 281:20140264Google Scholar
  410. Shinmyo Y, Mito T, Uda T, Nakamura T, Miyawaki K, Ohuchi H, Noji S (2006) brachyenteron is necessary for morphogenesis of the posterior gut but not for anteroposterior axial elongation from the posterior growth zone in the intermediate-germband cricket Gryllus bimaculatus. Development 133:4539–4547PubMedGoogle Scholar
  411. Shippy TD, Guo J, Brown SJ, Beeman RW, Denell RE (2000) Analysis of maxillopedia expression pattern and larval cuticular phenotype in wild-type and mutant Tribolium. Genetics 155:721–731PubMedCentralPubMedGoogle Scholar
  412. Shippy TD, Ronshaugen M, Cande J, He J, Beeman RW, Levine M, Brown SJ, Denell RE (2008) Analysis of the Tribolium homeotic complex: insights into mechanisms constraining insect Hox clusters. Dev Genes Evol 218:127–139PubMedCentralPubMedGoogle Scholar
  413. Shippy TD, Yeager SJ, Denell RE (2009) The Tribolium spineless ortholog specifies both larval and adult antennal identity. Dev Genes Evol 219:45–51PubMedCentralPubMedGoogle Scholar
  414. Shirai LT, Saenko SV, Keller RA, Jerónimo MA, Brakefield PM, Descimon H, Wahlberg N, Beldade P (2012) Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol Biol 12:21PubMedCentralPubMedGoogle Scholar
  415. Simonnet F, Moczek AP (2011) Conservation and diversification of gene function during mouthpart development in Onthophagus beetles. Evol Dev 13:280–289PubMedGoogle Scholar
  416. Singer JB, Harbecke R, Kusch T, Reuter R, Lengyel JA (1996) Drosophila brachyenteron regulates gene activity and morphogenesis in the gut. Development 122:3707–3718PubMedGoogle Scholar
  417. Smith FW, Jockusch EL (2014) Hox genes require homothorax and extradenticle for body wall identity specification but not for appendage identity specification during metamorphosis of Tribolium castaneum. Dev Biol 395:182–197PubMedGoogle Scholar
  418. Smith FW, Angelini DR, Jockusch EL (2014) A functional genetic analysis in flour beetles (Tenebrionidae) reveals an antennal identity specification mechanism active during metamorphosis in Holometabola. Mech Dev 132:13–27PubMedGoogle Scholar
  419. Smith-Bolton RK, Worley MI, Kanda H, Hariharan IK (2009) Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev Cell 16:797–809PubMedCentralPubMedGoogle Scholar
  420. Snodgrass RE (1930) Insects: their ways and means of living. Smithson Sci Ser 5:1–362Google Scholar
  421. Snodgrass RE (1931) Morphology of the insect abdomen. Part I. General structure of the abdomen and its appendages. Smithson Misc Collect 85:1–128Google Scholar
  422. Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill, New YorkGoogle Scholar
  423. Sotillos S, De Celis JF (2005) Interactions between the Notch, EGFR, and decapentaplegic signaling pathways regulate vein differentiation during Drosophila pupal wing development. Dev Dyn 232:738–752PubMedGoogle Scholar
  424. Stansbury MS, Moczek AP (2014) The function of Hox and appendage-patterning genes in the development of an evolutionary novelty, the Photuris firefly lantern. Proc R Soc B Biol Sci 281:20133333Google Scholar
  425. Stark J, Bonacum J, Remsen J, DeSalle R (1999) The evolution and development of dipteran wing veins: a systematic approach. Annu Rev Entomol 44:97–129PubMedGoogle Scholar
  426. Stauber M, Jackle H, Schmidt-Ott U (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci 96:3786–3789PubMedCentralPubMedGoogle Scholar
  427. Stern DL (1998) A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396:463–466PubMedCentralPubMedGoogle Scholar
  428. Stern DL (2003) The Hox gene Ultrabithorax modulates the shape and size of the third leg of Drosophila by influencing diverse mechanisms. Dev Biol 256:355–366PubMedGoogle Scholar
  429. Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323:746–751PubMedCentralPubMedGoogle Scholar
  430. Stevens KE, Mann RS (2007) A balance between two nuclear localization sequences and a nuclear export sequence governs Extradenticle subcellular localization. Genetics 175:1625–1636PubMedCentralPubMedGoogle Scholar
  431. Struhl G (1982) Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A 79:7380–7384PubMedCentralPubMedGoogle Scholar
  432. Stuart JJ, Brown SJ, Beeman RW, Denell RE (1991) A deficiency of the homeotic complex of the beetle Tribolium. Nature 350:72–74PubMedGoogle Scholar
  433. Suzanne M, Estella C, Calleja M, Sánchez-Herrero E (2003) The hernandez and fernandez genes of Drosophila specify eye and antenna. Dev Biol 260:465–483PubMedGoogle Scholar
  434. Suzuki Y, Palopoli M (2001) Evolution of insect abdominal appendages: are prolegs homologous or convergent traits? Dev Genes Evol 211:486–492PubMedGoogle Scholar
  435. 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 326:60–67PubMedCentralPubMedGoogle Scholar
  436. Svácha P (1992) What are and what are not imaginal discs: reevaluation of some basic concepts (Insecta, Holometabola). Dev Biol 154:101–117PubMedGoogle Scholar
  437. Svendsen PC, Formaz-Preston A, Leal SM, Brook WJ (2009) The Tbx20 homologs midline and H15 specify ventral fate in the Drosophila melanogaster leg. Development 136:2689–2693PubMedGoogle Scholar
  438. Tajiri R, Misaki K, Yonemura S, Hayashi S (2011) Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila. Development 138:4621–4626PubMedCentralPubMedGoogle Scholar
  439. 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 54:227–240PubMedGoogle Scholar
  440. Takashima S, Murakami R (2001) Regulation of pattern formation in the Drosophila hindgut by wg, hh, dpp, and en. Mech Dev 101:79–90PubMedGoogle Scholar
  441. Tanaka K, Truman JW (2005) Development of the adult leg epidermis in Manduca sexta: contribution of different larval cell populations. Dev Genes Evol 215:78–89PubMedGoogle Scholar
  442. Tanaka K, Truman JW (2007) Molecular patterning mechanism underlying metamorphosis of the thoracic leg in Manduca sexta. Dev Biol 305:539–550PubMedGoogle Scholar
  443. Tanaka K, Barmina O, Sanders LE, Arbeitman MN, Kopp A (2011) Evolution of sex-specific traits through changes in HOX-dependent doublesex expression. PLoS Biol 9:e1001131PubMedCentralPubMedGoogle Scholar
  444. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S, Albrechtsen M, An C, Aymeric J-L, Barthel A et al (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231–245PubMedGoogle Scholar
  445. Toegel JP, Wimmer EA, Prpic N-M (2009) Loss of spineless function transforms the Tribolium antenna into a thoracic leg with pretarsal, tibiotarsal, and femoral identity. Dev Genes Evol 219:53–58PubMedGoogle Scholar
  446. Tomita S, Kikuchi A (2009) Abd-B suppresses lepidopteran proleg development in posterior abdomen. Dev Biol 328:403–409PubMedGoogle Scholar
  447. Tomoyasu Y, Denell RE (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 214:575–578PubMedGoogle Scholar
  448. Tomoyasu Y, Wheeler SR, Denell RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433:643–647PubMedGoogle Scholar
  449. Tomoyasu Y, Arakane Y, Kramer KJ, Denell RE (2009) Repeated co-options of exoskeleton formation during wing-to-elytron evolution in beetles. Curr Biol 19:2057–2065PubMedGoogle Scholar
  450. Treisman JE (1999) A conserved blueprint for the eye? Bioessays 21:843–850PubMedGoogle Scholar
  451. Treisman JE, Rubin GM (1995) wingless inhibits morphogenetic furrow movement in the Drosophila eye disc. Development 121:3519–3527PubMedGoogle Scholar
  452. True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647Google Scholar
  453. True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3:109–119PubMedGoogle Scholar
  454. True JR, Edwards KA, Yamamoto D, Carroll SB (1999) Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr Biol 9:1382–1391PubMedGoogle Scholar
  455. Trueman JWH (1990) Comment—evolution of insect wings: a limb exite plus endite model. Can J Zool 68:1333–1335Google Scholar
  456. Truman JW, Ball EE (1998) Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects. Dev Genes Evol 208:357–368PubMedGoogle Scholar
  457. Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447–452PubMedGoogle Scholar
  458. Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 47:467–500PubMedGoogle Scholar
  459. Tsai Y, Yao J, Chen P, Posakony JW, Barolo S, Kim J, Henry Sun Y (2007) Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev Biol 306:760–771PubMedGoogle Scholar
  460. Turchyn N, Chesebro J, Hrycaj S, Couso JP, Popadić A (2011) Evolution of nubbin function in hemimetabolous and holometabolous insect appendages. Dev Biol 357:83–95PubMedCentralPubMedGoogle Scholar
  461. Ueno K, Hui CC, Fukuta M, Suzuki Y (1992) Molecular analysis of the deletion mutants in the E homeotic complex of the silkworm Bombyx mori. Development 114:555–563PubMedGoogle Scholar
  462. Ungerer P, Scholtz G (2008) Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata. Proc R Soc B: Biol Sci 275:369–376Google Scholar
  463. Ungerer P, Eriksson BJ, Stollewerk A (2011) Neurogenesis in the water flea Daphnia magna (Crustacea, Branchiopoda) suggests different mechanisms of neuroblast formation in insects and crustaceans. Dev Biol 357:42–52PubMedGoogle Scholar
  464. Vachon G, Cohen B, Pfeifle C, McGuffin ME, Botas J, Cohen SM (1992) Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell 71:437–450PubMedGoogle Scholar
  465. van der Zee M, Stockhammer O, von Levetzow C, da Fonseca RN, Roth S (2006) Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proc Natl Acad Sci 103:16307–16312PubMedCentralPubMedGoogle Scholar
  466. Wang C-W, Sun YH (2012) Segregation of eye and antenna fates maintained by mutual antagonism in Drosophila. Development 139:3413–3421PubMedGoogle Scholar
  467. Wang S-H, Simcox A, Campbell G (2000) Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev 14:2271–2276PubMedCentralPubMedGoogle Scholar
  468. Warren RW, Nagy L, Selegue J, Gates J, Carroll S (1994) Evolution of homeotic gene regulation and function in flies and butterflies. Nature 372:458–461PubMedGoogle Scholar
  469. Wasik BR, Moczek AP (2012) pangolin expression influences the development of a morphological novelty: beetle horns. Genesis 50:404–414PubMedCentralPubMedGoogle Scholar
  470. Wasik BR, Rose DJ, Moczek AP (2010) Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner. Evol Dev 12:353–362PubMedGoogle Scholar
  471. Werner T, Koshikawa S, Williams TM, Carroll SB (2010) Generation of a novel wing colour pattern by the wingless morphogen. Nature 464:1143–1148PubMedGoogle Scholar
  472. Wheat CW, Wahlberg N (2013) Phylogenomic insights into the Cambrian explosion, the colonization of land and the evolution of flight in Arthropoda. Syst Biol 62:93–109PubMedGoogle Scholar
  473. Wheeler SR, Carrico ML, Wilson BA, Brown SJ, Skeath JB (2003) The expression and function of the achaete-scute genes in Tribolium castaneum reveals conservation and variation in neural pattern formation and cell fate specification. Development 130:4373–4381PubMedGoogle Scholar
  474. Wigglesworth VB (1973) Evolution of insect wings and flight. Nature 246:127–129Google Scholar
  475. Wigglesworth VB (1976) The evolution of insect flight. In: Rainey RC (ed) Insect flight. Blackwell Scientific, OxfordGoogle Scholar
  476. Williams JA, Paddock SW, Carroll SB (1993) Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117:571–584PubMedGoogle Scholar
  477. Wirz J, Fessler LI, Gehring WJ (1986) Localization of the Antennapedia protein in Drosophila embryos and imaginal discs. EMBO J 5:3327–3334PubMedCentralPubMedGoogle Scholar
  478. Wittkopp PJ, Beldade P (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 20:65–71PubMedGoogle Scholar
  479. Wu J, Cohen SM (1999) Proximodistal axis formation in the Drosophila leg: subdivision into proximal and distal domains by Homothorax and Distal-less. Development 126:109–117PubMedGoogle Scholar
  480. Wu J, Cohen SM (2002) Repression of Teashirt marks the initiation of wing development. Development 129:2411–2418PubMedGoogle Scholar
  481. Xiang H, Li MW, Guo JH, Jiang JH, Huang YP (2011) Influence of RNAi knockdown for E-complex genes on the silkworm proleg development. Arch Insect Biochem Physiol 76:1–11PubMedGoogle Scholar
  482. Yamada A, Martindale MQ, Fukui A, Tochinai S (2010) Highly conserved functions of the Brachyury gene on morphogenetic movements: insight from the early-diverging phylum Ctenophora. Dev Biol 339:212–222PubMedGoogle Scholar
  483. Yamamoto DS, Sumitani M, Tojo K, Lee JM, Hatakeyama M (2004) Cloning of a decapentaplegic orthologue from the sawfly, Athalia rosae (Hymenoptera), and its expression in the embryonic appendages. Dev Genes Evol 214:128–133PubMedGoogle Scholar
  484. Yan S-J, Zartman JJ, Zhang M, Scott A, Shvartsman SY, Li WX (2009) Bistability coordinates activation of the EGFR and DPP pathways in Drosophila vein differentiation. Mol Syst Biol 5:278PubMedCentralPubMedGoogle Scholar
  485. Yang X, ZarinKamar N, Bao R, Friedrich M (2009a) Probing the Drosophila retinal determination gene network in Tribolium (I): the early retinal genes dachshund, eyes absent and sine oculis. Dev Biol 333:202–214PubMedGoogle Scholar
  486. Yang X, Weber M, ZarinKamar N, Posnien N, Friedrich F, Wigand B, Beutel R, Damen WG, Bucher G, Klingler M (2009b) Probing the Drosophila retinal determination gene network in Tribolium (II): the Pax6 genes eyeless and twin of eyeless. Dev Biol 333:215–227PubMedGoogle Scholar
  487. Yasukochi Y, Ashakumary LA, Wu C, Yoshido A, Nohata J, Mita K, Sahara K (2004) Organization of the Hox gene cluster of the silkworm, Bombyx mori: a split of the Hox cluster in a non-Drosophila insect. Dev Genes Evol 214:606–614PubMedGoogle Scholar
  488. Yeh S-D, Liou S-R, True JR (2006) Genetics of divergence in male wing pigmentation and courtship behavior between Drosophila elegans and D. gunungcola. Heredity (Edinb) 96:383–395Google Scholar
  489. Yokoyama H, Ogino H, Stoick-Cooper CL, Grainger RM, Moon RT (2007) Wnt/β-catenin signaling has an essential role in the initiation of limb regeneration. Dev Biol 306:170–178PubMedCentralPubMedGoogle Scholar
  490. Yoshiyama N, Tojo K, Hatakeyama M (2013) A survey of the effectiveness of non-cell autonomous RNAi throughout development in the sawfly, Athalia rosae (Hymenoptera). J Insect Physiol 59:400–407PubMedGoogle Scholar
  491. Yue C, Hua B (2010) Are abdominal prolegs serially homologous with the thoracic legs in Panorpidae (Insecta: Mecoptera)? Embryological evidence. J Morphol 271:1366–1373PubMedGoogle Scholar
  492. 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 2:1–15Google Scholar
  493. Zecca M, Struhl G (2002) Control of growth and patterning of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development 129:1369–1376Google Scholar
  494. Zecca M, Struhl G (2007) Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation. Development 134:3001–3010PubMedGoogle Scholar
  495. Zecca M, Basler K, Struhl G (1995) Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121:2265–2278PubMedGoogle Scholar
  496. Zera AJ (2004) The endocrine regulation of wing polymorphism in insects: state of the art, recent surprises, and future directions. Integr Comp Biol 43:607–616Google Scholar
  497. Zhang H, Shinmyo Y, Mito T, Miyawaki K, Sarashina I, Ohuchi H, Noji S (2005) Expression patterns of the homeotic genes Scr, Antp, Ubx, and abd-A during embryogenesis of the cricket Gryllus bimaculatus. Gene Expr Patterns 5:491–502PubMedGoogle Scholar
  498. Zhang XG, Siveter DJ, Waloszek D, Maas A (2007) An epipodite-bearing crown-group crustacean from the lower Cambrian. Nature 449:595–598PubMedGoogle Scholar
  499. Zhurov V, Terzin T, Grbić M (2004) Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432:764–769PubMedGoogle Scholar
  500. Zirin JD, Mann RS (2007) Nubbin and Teashirt mark barriers to clonal growth along the proximal – distal axis of the Drosophila wing. Dev Biol 304:745–758PubMedCentralPubMedGoogle Scholar

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© Springer-Verlag Wien 2015

Authors and Affiliations

  1. 1.Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA
  2. 2.Biology DepartmentThe University of North Carolina at Chapel HillChapel HillUSA

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