Genetics, development and composition of the insect head - A beetle's view

Arthropod Structure and Development

Volumn 39, Issue 6, 2010, Pages 399-410

  Posnien, Nico ^a   Schinko, Johannes B ^b   Kittelmann, Sebastian ^c   Bucher, Gregor ^c  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Acron; Bend and zipper; Intercalary; Labrum; Orthodenticle; Six3

Indexed keywords

BEETLE; DEVELOPMENTAL GENE; DROSOPHILA MELANOGASTER; GENE CONTROL; GENETIC VARIABILITY; HEAD; INSECT GENETICS; MORPHOGENESIS; NONHUMAN; ONTOGENY; REVIEW;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; HEAD; MODELS, ANIMAL; TRIBOLIUM;

CHLOROCRAMBE HASTATA; COLEOPTERA; DROSOPHILA MELANOGASTER; HEXAPODA; TRIBOLIUM (BEETLE); TRIBOLIUM CASTANEUM;

EID: 78649688669     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.asd.2010.08.002     Document Type: Review

References (143)

1. Abzhanov A., Kaufman T.C. Homeotic genes and the arthropod head: expression patterns of the labial, proboscipedia, and deformed genes in crustaceans and insects. Proceedings of the National Academy of Sciences USA 1999, 96:10224-10229.
2. Aguinaldo A.M., Turbeville J.M., Linford L.S., Rivera M.C., Garey J.R., Raff R.A., Lake J.A. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997, 387:489-493.
3. Akiyama-Oda Y., Oda H. Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 2006, 133:2347-2357.
4. Amdam G.V., Simoes Z.L., Guidugli K.R., Norberg K., Omholt S.W. Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnology 2003, 3:1.
5. Angelini D.R., Liu P.Z., Hughes C.L., Kaufman T.C. Hox gene function and interaction in the milkweed bug Oncopeltus fasciatus (Hemiptera). Developmental Biology 2005, 287:440-455.
6. Arendt D., Denes A.S., Jekely G., Tessmar-Raible K. The evolution of nervous system centralization. Philosophical Transactions of the Royal Society B: Biological Sciences 2008, 363:1523-1528.
7. Berghammer A.J., Klingler M., Wimmer E.A. A universal marker for transgenic insects. Nature 1999, 402:370-371.
8. Bitsch J., Bitsch C. The tritocerebrum and the clypeolabrum in mandibulate arthropods: segmental interpretations. Acta Zoologica 2010, 91:249-266.
9. Boyan G.S., Bräunig P., Posser S., Williams J.L.D. Embryonic development of the sensory innervation of the clypeo-labral complex: further support for serially homologous appendages in the locust. Arthropod Structure & Development 2003, 32:289-302.
10. Boyan G.S., Williams J.L., Posser S., Bräunig P. Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthropod Structure & Development 2002, 31:65-76.
11. Brown S., DeCamillis M., Gonzalez-Charneco K., Denell M., Beeman R., Nie W., Denell R. Implications of the Tribolium deformed mutant phenotype for the evolution of Hox gene function. Proceedings of the National Academy of Sciences USA 2000, 97:4510-4514.
12. Brown S., Fellers J., Shippy T., Denell R., Stauber M., Schmidt-Ott U. A strategy for mapping bicoid on the phylogenetic tree. Current Biology 2001, 11:R43-R44.
13. Brown S.J., Mahaffey J.P., Lorenzen M.D., Denell R.E., Mahaffey J.W. Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evolution & Development 1999, 1:11-15.
14. Brown S.J., Patel N.H., Denell R.E. Embryonic expression of the single Tribolium engrailed homolog. Developmental Genetics 1994, 15:7-18.
15. Brown S.J., Shippy T.D., Beeman R.W., Denell R.E. Tribolium Hox genes repress antennal development in the gnathos and trunk. Molecular Phylogenetics and Evolution 2002, 24:384-387.
16. Brusca R.C., Brusca G.J. Invertebrates 2003, Sinauer Associates, Sunderland. second ed.
17. Bucher G., Farzana L., Brown S.J., Klingler M. Anterior localization of maternal mRNAs in a short germ insect lacking bicoid. Evolution & Development 2005, 7:142-149.
18. Bucher G., Klingler M. Tribolium mae expression suggests roles in terminal and midline patterning and in the specification of mesoderm. Development Genes and Evolution 2005, 215:478-481.
19. Bucher G., Scholten J., Klingler M. Parental RNAi in Tribolium (Coleoptera). Current Biology 2002, 12:R85-R86.
20. Budd G.E. A palaeontological solution to the arthropod head problem. Nature 2002, 417:271-275.
21. Cerny A.C., Grossmann D., Bucher G., Klingler M. The Tribolium ortholog of knirps and knirps-related is crucial for head segmentation but plays a minor role during abdominal patterning. Developmental Biology 2008, 321:284-294.
22. Chaudonneret J. La morphologie céphalique de Thermobia domestica (Packard) (Insecte Aptérygote Thysanoure). Annales Des Sciences Naturelles, Zoologie 1950, 11:145-302.
23. Chesebro J., Hrycaj S., Mahfooz N., Popadic A. Diverging functions of Scr between embryonic and post-embryonic development in a hemimetabolous insect, Oncopeltus fasciatus. Developmental Biology 2009, 329:142-151.
24. Chipman A.D., Arthur W., Akam M. A double segment periodicity underlies segment generation in centipede development. Current Biology 2004, 14:1250-1255.
25. Choe C.P., Brown S.J. Evolutionary flexibility of pair-rule patterning revealed by functional analysis of secondary pair-rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum. Developmental Biology 2007, 302:281-294.
26. Choe C.P., Miller S.C., Brown S.J. A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proceedings of the National Academy of Sciences USA 2006, 103:6560-6564.
27. Clements J., Lu Z., Gehring W.J., Meinertzhagen I.A., Callaerts P. Central projections of photoreceptor axons originating from ectopic eyes in Drosophila. Proceedings of the National Academy of Sciences USA 2008.
28. Cohen S.M., Jurgens G. Mediation of Drosophila head development by gap-like segmentation genes. Nature 1990, 346:482-485.
29. Weinstock G.M., Robinson G.E. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949. and the Honeybee Genome Sequencing Consortium.
30. Werren J.H. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327:343-348. and the Nasonia Genome Working Group.
31. Crozatier M., Valle D., Dubois L., Ibnsouda S., Vincent A. Collier, a novel regulator of Drosophila head development, is expressed in a single mitotic domain. Current Biology 1996, 6:707-718.
32. Dalton D., Chadwick R., McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes and Development 1989, 3:1940-1956.
33. Damen W.G., Hausdorf M., Seyfarth E.A., Tautz D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proceedings of the National Academy of Sciences USA 1998, 95:10665-10670.
34. Dearden P.K., Akam M. Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, decapentaplegic and caudal expression. Development 2001, 128:3435-3444.
35. Dearden P.K., Wilson M.J., Sablan L., Osborne P.W., Havler M., McNaughton E., Kimura K., Milshina N.V., Hasselmann M., Gempe T., Schioett M., Brown S.J., Elsik C.G., Holland P.W., Kadowaki T., Beye M. Patterns of conservation and change in honey bee developmental genes. Genome Research 2006, 16:1376-1384.
36. DeCamillis M., ffrench-Constant R. Proboscipedia represses distal signaling in the embryonic gnathal limb fields of Tribolium castaneum. Development Genes and Evolution 2003, 213:55-64.
37. DeCamillis M.A., Lewis D.L., Brown S.J., Beeman R.W., Denell R.E. Interactions of the Tribolium sex combs reduced and proboscipedia orthologs in embryonic labial development. Genetics 2001, 159:1643-1648.
38. Economou A.D., Telford M.J. Comparative gene expression in the heads of Drosophila melanogaster and Tribolium castaneum and the segmental affinity of the Drosophila hypopharyngeal lobes. Evolution & Development 2009, 11:88-96.
39. Eriksson B.J., Larson E.T., Thornqvist P.O., Tait N.N., Budd G.E. Expression of engrailed in the developing brain and appendages of the onychophoran Euperipatoides kanangrensis (Reid). Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2005, 304:220-228.
40. Eriksson B.J., Tait N.N., Budd G.E., Janssen R., Akam M. Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Development Genes and Evolution 2010.
41. Evans C.J., Olson J.M., Ngo K.T., Kim E., Lee N.E., Kuoy E., Patananan A.N., Sitz D., Tran P., Do M.T., Yackle K., Cespedes A., Hartenstein V., Call G.B., Banerjee U. G-TRACE: rapid Gal4-based cell lineage analysis in Drosophila. Nature Methods 2009, 6:603-605.
42. Ferris G.F. Some observations on the head of insects. Microentomology 1942, 7:25-62.
43. Freitas R., Zhang G., Cohn M.J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 2006, 442:1033-1037.
44. Gallitano-Mendel A., Finkelstein R. Novel segment polarity gene interactions during embryonic head development in Drosophila. Developmental Biology 1997, 192:599-613.
45. Gallitano-Mendel A., Finkelstein R. Ectopic orthodenticle expression alters segment polarity gene expression but not head segment identity in the Drosophila embryo. Developmental Biology 1998, 199:125-137.
46. Gao Q., Wang Y., Finkelstein R. Orthodenticle regulation during embryonic head development in Drosophila. Mechanisms of Development 1996, 56:3-15.
47. Giribet G. Molecules, development and fossils in the study of metazoan evolution; Articulata vs. Ecdysozoa revisited. Zoology (Jena) 2003, 106:303-326.
48. Giribet G. Assembling the lophotrochozoan (=spiralian) tree of life. Philosophical Transactions of the Royal Society B: Biological Sciences 2008, 363:1513-1522.
49. Goltsev Y., Hsiong W., Lanzaro G., Levine M. Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Developmental Biology 2004, 275:435-446.
50. Gonzalez-Gaitan M., Rothe M., Wimmer E.A., Taubert H., Jackle H. Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures. Proceedings of the National Academy of Sciences USA 1994, 91:8567-8571.
51. Gonzalez-Reyes A., Morata G. The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products. Cell 1990, 61:515-522.
52. Gorfinkiel N., Morata G., Guerrero I. The homeobox gene distal-less induces ventral appendage development in Drosophila. Genes and Development 1997, 11:2259-2271.
53. Grossniklaus U., Cadigan K.M., Gehring W.J. Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 1994, 120:3155-3171.
54. Grossniklaus U., Pearson R.K., Gehring W.J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes and Development 1992, 6:1030-1051.
55. Gruner H.E., Hartmann-Schröder G., Kilias R., Moritz M. Wirbellose Tiere 1993, Gustav Fischer Verlag, Jena, Stuttgart, New York.
56. Haas M.S., Brown S.J., Beeman R.W. Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum. Development Genes and Evolution 2001, 211:96-102.
57. Haas M.S., Brown S.J., Beeman R.W. Pondering the procephalon: the segmental origin of the labrum. Development Genes and Evolution 2001, 211:89-95.
58. Halder G., Callaerts P., Gehring W.J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995, 267:1788-1792.
59. Hrycaj S., Chesebro J., Popadic A. Functional analysis of Scr during embryonic and post-embryonic development in the cockroach, Periplaneta americana. Developmental Biology 2010, 341:324-334.
60. Hughes C.L., Kaufman T.C. 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 2000, 127:3683-3694.
61. Jager M., Murienne J., Clabaut C., Deutsch J., Le Guyader H., Manuel M. Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider. Nature 2006, 441:506-508.
62. Janssen R., Damen W.G. The ten Hox genes of the millipede Glomeris marginata. Development Genes and Evolution 2006, 216:451-465.
63. Jurgens G., Lehmann R., Schardin M., Nüsslein-Volhard C. Segmental organisation of the head in the embryo of Drosophila melanogaster. Roux's Archives of Developmental Biology 1986, 195:359-377.
64. Kimm M.A., Prpic N.M. Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia. Zoomorphology 2006, 125:147-155.
65. Klingler M., Erdelyi M., Szabad J., Nüsslein-Volhard C. Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature 1988, 335:275-277.
66. Lagutin O.V., Zhu C.C., Kobayashi D., Topczewski J., Shimamura K., Puelles L., Russell H.R., McKinnon P.J., Solnica-Krezel L., Oliver G. Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes and Development 2003, 17:368-379.
67. Lemke S., Schmidt-Ott U. Evidence for a composite anterior determinant in the hover fly Episyrphus balteatus (Syrphidae), a cyclorrhaphan fly with an anterodorsal serosa anlage. Development 2009, 136:117-127.
68. Li Y., Brown S.J., Hausdorf B., Tautz D., Denell R.E., Finkelstein R. Two orthodenticle-related genes in the short germ beetle Tribolium castaneum. Development Genes and Evolution 1996, 206:35-45.
69. Liaw G.J., Lengyel J.A. Control of tailless expression by bicoid, dorsal and synergistically interacting terminal system regulatory elements. Mechanisms of Development 1993, 40:47-61.
70. Liu P.Z., Kaufman T.C. Hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 2004, 131:1515-1527.
71. Liu P.Z., Kaufman T.C. even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 2005, 132:2081-2092.
72. Liubicich D.M., Serano J.M., Pavlopoulos A., Kontarakis Z., Protas M.E., Kwan E., Chatterjee S., Tran K.D., Averof M., Patel N.H. Knockdown of parhyale ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proceedings of the National Academy of Sciences USA 2009, 106:13892-13896.
73. Lowe C.J., Wu M., Salic A., Evans L., Lander E., Stange-Thomann N., Gruber C.E., Gerhart J., Kirschner M. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 2003, 113:853-865.
74. Lynch J.A., Brent A.E., Leaf D.S., Pultz M.A., Desplan C. Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 2006, 439:728-732.
75. Lynch J.A., Desplan C. A method for parental RNA interference in the wasp Nasonia vitripennis. Nature Protocols 2006, 1:486-494.
76. Martin J.R., Raibaud A., Ollo R. Terminal pattern elements in Drosophila embryo induced by the torso-like protein. Nature 1994, 367:741-745.
77. Merrill V.K., Diederich R.J., Turner F.R., Kaufman T.C. A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophila melanogaster. Developmental Biology 1989, 135:376-391.
78. Miyawaki K., Mito T., Sarashina I., Zhang H., Shinmyo Y., Ohuchi H., Noji S. Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mechanisms of Development 2004, 121:119-130.
79. Mohler J. Spatial regulation of segment polarity gene expression in the anterior terminal region of the Drosophila blastoderm embryo. Mechanisms of Development 1995, 50:151-161.
80. Mohler J., Vani K., Leung S., Epstein A. Segmentally restricted, cephalic expression of a leucine zipper gene during Drosophila embryogenesis. Mechanisms of Development 1991, 34:3-9.
81. Nagy L.M., Carroll S. Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature 1994, 367:460-463.
82. Nakao H. Characterization of Bombyx embryo segmentation process: expression profiles of engrailed, even-skipped, caudal, and wnt1/wingless homologues. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2010, 314:224-231.
83. Nie W., Stronach B., Panganiban G., Shippy T., Brown S., Denell R. Molecular characterization of Tclabial and the 3′ end of the Tribolium homeotic complex. Development Genes and Evolution 2001, 211:244-251.
84. Nielsen C. Animal Evolution, Interrelationships of the Living Phyla 2001, Oxford University Press, Oxford. second ed.
85. Nunes da Fonseca R., von Levetzow C., Kalscheuer P., Basal A., van der Zee M., Roth S. Self-regulatory circuits in dorsoventral axis formation of the short-germ beetle Tribolium castaneum. Developmental Cell 2008, 14:605-615.
86. Pankratz M.J., Jackle H. Making stripes in the Drosophila embryo. Trends in Genetics 1990, 6:287-292.
87. Patel N.H., Kornberg T.B., Goodman C.S. Expression of engrailed during segmentation in grasshopper and crayfish. Development 1989, 107:201-212.
88. Pavlopoulos A., Averof M. Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. Proceedings of the National Academy of Sciences USA 2005, 102:7888-7893.
89. Peterson M.D., Popadic A., Kaufman T.C. The expression of two engrailed-related genes in an apterygote insect and a phylogenetic analysis of insect engrailed-related genes. Development Genes and Evolution 1998, 208:547-557.
90. Posnien N., Bashasab F., Bucher G. The insect upper lip (labrum) is a nonsegmental appendage-like structure. Evolution & Development 2009, 11:479-487.
91. Posnien N., Bucher G. Formation of the insect head involves lateral contribution of the intercalary segment, which depends on Tc-labial function. Developmental Biology 2010, 338:107-116.
92. Reichert H. Evolutionary conservation of mechanisms for neural regionalization, proliferation and interconnection in brain development. Biological Letters 2009, 5:112-116.
93. Reichert H., Simeone A. Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philosophical Transactions of the Royal Society B: Biological Sciences 2001, 356:1533-1544.
94. Rempel G.J. The evolution of the insect head: the endless dispute. Quaestiones Entomologicae 1975, 11:7-25.
95. Richards S. The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452:949-955. and the Tribolium Genome Sequencing Consortium.
96. Rogers B.T., Kaufman T.C. Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 1996, 122:3419-3432.
97. Rogers B.T., Kaufman T.C. Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. International Reviews in Cytology 1997, 174:1-84.
98. Rogers B.T., Peterson M.D., Kaufman T.C. The development and evolution of insect mouth parts as revealed by the expression patterns of gnathocephalic genes. Evolution & Development 2002, 4:96-110.
99. Sander K. Specification of the basic body pattern in insect embryogenesis. Advances in Insect Physology 1976, 125-238. Academic Press, Cambridge. J.E. Treherne, M.J. Berridge, V.B. Wigglesworth (Eds.).
100. Schaeffer V., Killian D., Desplan C., Wimmer E.A. High bicoid levels render the terminal system dispensable for Drosophila head development. Development 2000, 127:3993-3999.
101. Schaeper N.D., Pechmann M., Damen W.G., Prpic N.M., Wimmer E.A. Evolutionary plasticity of collier function in head development of diverse arthropods. Developmental Biology 2010, 344:363-376.
102. Schaeper N.D., Prpic N.M., Wimmer E.A. A clustered set of three Sp-family genes is ancestral in the Metazoa: evidence from sequence analysis, protein domain structure, developmental expression patterns and chromosomal location. BMC Evol Biol. 2010, 30(10):88.
103. Schetelig M.F., Schmid B.G., Zimowska G., Wimmer E.A. Plasticity in mRNA expression and localization of orthodenticle within higher Diptera. Evolution & Development 2008, 10:700-704.
104. Schinko J.B., Kreuzer N., Offen N., Posnien N., Wimmer E.A., Bucher G. Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Developmental Biology 2008, 317:600-613.
105. Schinko J.B., Weber M., Viktorinova I., Kiupakis A., Averof M., Klingler M., Wimmer E.A., Bucher G. Functionality of the GAL4/UAS system in Tribolium requires the use of endogenous core promoters. BMC Developmental Biology 2010, 10:53.
106. Schmidt-Ott U., Gonzalez-Gaitan M., Jackle H., Technau G.M. Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proceedings of the National Academy of Sciences USA 1994, 91:8363-8367.
107. Schmidt-Ott U., Technau G.M. Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 1992, 116:111-125.
108. Schmidt-Ott U., Technau G.M. Fate-mapping in the procephalic region of the embryonic Drosophila head. Roux's Archives of Developmental Biology 1994, 203:367-373.
109. Schock F., Reischl J., Wimmer E., Taubert H., Purnell B.A., Jackle H. Phenotypic suppression of empty spiracles is prevented by buttonhead. Nature 2000, 405:351-354.
110. Scholtz G., Edgecombe G.D. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Development Genes and Evolution 2006, 216:395-415.
111. Schoppmeier M., Fischer S., Schmitt-Engel C., Löhr U., Klingler M. An ancient anterior patterning system promotes caudal repression and head formation in ecdysozoa. Current Biology 2009, 19:1811-1815.
112. Schoppmeier M., Schroder R. Maternal torso signaling controls body axis elongation in a short germ insect. Current Biology 2005, 15:2131-2136.
113. Schroder R. The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 2003, 422:621-625.
114. Schroder R., Eckert C., Wolff C., Tautz D. Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proceedings of the National Academy of Sciences USA 2000, 97:6591-6596.
115. Shippy T.D., Rogers C.D., Beeman R.W., Brown S.J., Denell R.E. The Tribolium castaneum ortholog of Sex combs reduced controls dorsal ridge development. Genetics 2006, 174:297-307.
116. Simpson-Brose M., Treisman J., Desplan C. Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 1994, 78:855-865.
117. Snodgrass R.E. Principles of Insect Morphology 1935, McGRaw Hill, New York.
118. Stauber M., Jackle H., Schmidt-Ott U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proceedings of the National Academy of Sciences USA 1999, 96:3786-3789.
119. Stauber M., Prell A., Schmidt-Ott U. A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proceedings of the National Academy of Sciences USA 2002, 99:274-279.
120. Technau G.M., Berger C., Urbach R. Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Developmental Dynamics 2006, 235:861-869.
121. Technau G.M., Campos-Ortega J.A. Fate-mapping in wildtype Drosophila melanogaster. II. Injections of horseradish peroxidase in cells of the early gastrula stage. Roux's Archieves of Developmental Biology 1985, 194:196-212.
122. Telford M.J., Bourlat S.J., Economou A., Papillon D., Rota-Stabelli O. The evolution of the ecdysozoa. Philosophical Transactions of the Royal Society B: Biological Sciences 2008, 363:1529-1537.
123. Telford M.J., Thomas R.H. Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proceedings of the National Academy of Sciences USA 1998, 95:10671-10675.
124. Tomoyasu Y., Denell R.E. Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Development Genes and Evolution 2004, 214:575-578.
125. Tomoyasu Y., Miller S.C., Tomita S., Schoppmeier M., Grossmann D., Bucher G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology 2008, 9:R10.
126. Trauner J., Schinko J., Lorenzen M.D., Shippy T.D., Wimmer E.A., Beeman R.W., Klingler M., Bucher G., Brown S.J. Large-scale insertional mutagenesis of a coleopteran stored grain pest, the red flour beetle Tribolium castaneum, identifies embryonic lethal mutations and enhancer traps. BMC Biology 2009, 7:73.
127. Urbach R., Technau G.M. Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect secies. Arthropod Structure & Development 2003, 32:103-123.
128. Urbach R., Technau G.M. Neuroblast formation and patterning during early brain development in Drosophila. Bioessays 2004, 26:739-751.
129. van der Zee M., Stockhammer O., von Levetzow C., Nunes da Fonseca R., Roth S. Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proceedings of the National Academy of Sciences USA 2006, 103:16307-16312.
130. Vincent A., Blankenship J.T., Wieschaus E. Integration of the head and trunk segmentation systems controls cephalic furrow formation in Drosophila. Development 1997, 124:3747-3754.
131. Wada S. Analyse der Kopf-Hals-Region von Tachycines (Saltatoria) in morphogenetische Einheiten. II. Mitteilung: Experimentell-teratologische Befunde am Kopfskelett mit Berücksichtigung des zentralen Nervensystems. Zool Jb Anat 1965, 83:235-326.
132. Walldorf U., Gehring W.J. Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. Embo Journal 1992, 11:2247-2259.
133. Waloszek D., Chen J., Maas A., Wang X. Early Cambrian arthropods - new insights into arthropod head and structural evolution. Arthropod Structure & Development 2005, 34:189-205.
134. Weber H. Grundriss der Insektenkunde 1966, Gustav Fischer Verlag, Stuttgart. fourth ed.
135. Westheide W., Rieger R. Spezielle Zoologie 2007, Gustav Fischer Verlag, Jena, Stuttgart, New York.
136. Wheeler S.R., Carrico M.L., Wilson B.A., Skeath J.B. The Tribolium columnar genes reveal conservation and plasticity in neural precursor patterning along the embryonic dorsal-ventral axis. Developmental Biology 2005, 279:491-500.
137. Williams J.L., Boyan G.S. Building the central complex of the grasshopper Schistocerca gregaria: axons pioneering the w, x, y, z tracts project onto the primary commissural fascicle of the brain. Arthropod Structure & Development 2008, 37:129-140.
138. Williams J.L., Güntner M., Boyan G. Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, x, y, z tracts. Arthropod Structure & Development 2005, 34:97-110.
139. Wilson M.J., Dearden P.K. Tailless patterning functions are conserved in the honeybee even in the absence of Torso signaling. Developmental Biology 2009, 335:276-287.
140. Wilson M.J., Havler M., Dearden P.K. Giant, Kruppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo. Developmental Biology 2010, 339:200-211.
141. Wimmer E.A., Cohen S.M., Jackle H., Desplan C. buttonhead does not contribute to a combinatorial code proposed for Drosophila head development. Development 1997, 124:1509-1517.
142. Wimmer E.A., Simpson-Brose M., Cohen S.M., Desplan C., Jackle H. Trans- and cis-acting requirements for blastodermal expression of the head gap gene buttonhead. Mechanisms of Development 1995, 53:235-245.
143. Yang X., Weber M., Zarinkamar N., Posnien N., Friedrich F., Wigand B., Beutel R., Damen W.G., Bucher G., Klingler M., Friedrich M. Probing the Drosophila retinal determination gene network in Tribolium (II): the Pax6 genes eyeless and twin of eyeless. Developmental Biology 2009, 333:215-227.