Abstract
By any criterion, Insecta (as a subtaxon of Hexapoda) is the most successful taxon on the planet (see Chaps. 2 and 3 for the inclusion of the various subtaxa in Hexapoda versus Insecta). The number of described insect species nears one million, and they are found in almost every ecosystem, forming the major component of animal biomass in most. Within the insects, the largest group comprises the holometabolous insects. In the holometabolous insects, the outcome of embryogenesis is a larva, which normally has a relatively simple morphology, with no wings or reproductive organs and either no legs or rudimentary legs. The larva goes through several molts, pupates, and undergoes metamorphosis within the pupa, finally hatching from the pupa as an adult with limbs, wings, and reproductive organs. Most of the remaining species belong to the hemimetabolous insects, a paraphyletic group wherein the outcome of embryogenesis is a nymph, superficially similar to an adult, but with no wings or reproductive organs. The nymph undergoes several molts, each being slightly larger and closer in shape and size to the adult, with the final adult molt developing wings and reproductive organs, without going through a pupal stage or undergoing a dramatic metamorphosis. Finally, a small group of insects undergoes ametabolous development, wherein there is no terminal adult stage, and the animal continues to molt even after developing reproductive organs. These insects are all primitively wingless.
Chapter vignette artwork by Brigitte Baldrian.© Brigitte Baldrian and Andreas Wanninger.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 1.
Although technically incorrect, the shorthand notation Drosophila rather than D. melanogaster has become accepted in the EvoDevo literature, and it is used herein.
References
Abmayr SM, Pavlath GK (2012) Myoblast fusion: lessons from flies and mice. Development 139:641–656
Affolter M, Caussinus E (2008) Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture. Development 135:2055–2064
Ainsworth C, Wan S, Skaer H (2000) Coordinating cell fate and morphogenesis in Drosophila renal tubules. Philos Trans R Soc Lond B Biol Sci 355:931–937
Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22
Andrew DJ, Ewald AJ (2010) Morphogenesis of epithelial tubes: insights into tube formation, elongation, and elaboration. Dev Biol 341:34–55
Andrew DJ, Henderson KD, Seshaiah P (2000) Salivary gland development in Drosophila melanogaster. Mech Dev 92:5–17
Bae YK, Trisnadi N, Kadam S, Stathopoulos A (2012) The role of FGF signaling in guiding coordinate movement of cell groups: guidance cue and cell adhesion regulator? Cell Adh Migr 6:397–403
Barrett K, Leptin M, Settleman J (1997) The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91:905–915
Barrett AL, Krueger S, Datta S (2008) Branchless and Hedgehog operate in a positive feedback loop to regulate the initiation of neuroblast division in the Drosophila larval brain. Dev Biol 317:234–245
Bate M (1993) The mesoderm and its derivatives. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 941–1012
Bate M, Rushton E, Currie DA (1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113:79–89
Baylies MK, Bate M, Ruiz Gomez M (1997) The specification of muscle in Drosophila. Cold Spring Harb Symp Quant Biol 62:385–393
Beckervordersandforth RM, Rickert C, Altenhein B, Technau GM (2008) Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression. Mech Dev 125:542–557
Bello BC, Izergina N, Caussinus E, Reichert H (2008) Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev 3:5
Betschinger J, Knoblich JA (2004) Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr Biol 14:R674–R685
Bhat KM (1999) Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. Bioessays 21:472–485
Bienz M (1994) Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet 10:22–26
Bodmer R, Barbel S, Sheperd S, Jack JW, Jan LY, Jan YN (1987) Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51:293–307
Bodmer R, Golden K, Lockwood WB, Ocorr KA, Park M, Su MT, Venkatesh TV (1997) Heart development in Drosophila. In: Wasserman P (ed) Advances in developmental biology, vol 5. JAI Press, Greenwich, pp 201–236
Borkowski OM, Brown NH, Bate M (1995) Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila. Development 121:4183–4193
Boyle M, DiNardo S (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121:1815–1825
Boyle M, Bonini N, DiNardo S (1997) Expression and function of clift in the development of somatic gonadal precursors within the Drosophila mesoderm. Development 124:971–982
Brody T, Odenwald WF (2005) Regulation of temporal identities during Drosophila neuroblast lineage development. Curr Opin Cell Biol 17:672–675
Broihier HT, Moore LA, Van Doren M, Newman S, Lehmann R (1998) Zfh-1 is required for germ cell migration and gonadal mesoderm development in Drosophila. Development 125:655–666
Bryantsev AL, Cripps RM (2009) Cardiac gene regulatory networks in Drosophila. Biochim Biophys Acta 1789:343–353
Buechling T, Akasaka T, Vogler G, Ruiz-Lozano P, Ocorr K, Bodmer R (2009) Non-autonomous modulation of heart rhythm, contractility and morphology in adult fruit flies. Dev Biol 328:483–492
Buff E, Carmena A, Gisselbrecht S, Jiménez F, Michelson AM (1998) Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development 125:2075–2086
Cagan R (1993) Cell fate specification in the developing Drosophila retina. Dev Suppl 1993:19–28
Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster, 2nd edn. Springer, Berlin/Heidelberg
Campos-Ortega JA, Jan YN (1991) Genetic and molecular bases of neurogenesis in Drosophila melanogaster. Annu Rev Neurosci 14:399–420
Carmena A, Bate M, Jiménez F (1995) Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 9:2373–2383
Carmena A, Murugasu-Oei B, Menon D, Jiménez F, Chia W (1998) Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev 12:304–315
Carmena A, Buff E, Halfon MS, Gisselbrecht S, Jiménez F, Baylies MK, Michelson AM (2002) Reciprocal regulatory interactions between the Notch and Ras signaling pathways in the Drosophila embryonic mesoderm. Dev Biol 244:226–242
Carratalá M, Vernós I, Ransom R, Marco R (1989) Modeling the regulation of the bithorax complex in Drosophila melanogaster: the phenotypic effects of Ubx, abd-A and Abd-B heterozygotic larvae, and a homozygous Ubx- abd A hybrid gene. Int J Dev Biol 33:455–466
Casanova J, Sánchez-Herrero E, Morata G (1986) Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell 47:627–636
Casares F, Sánchez-Herrero E (1995) Regulation of the infraabdominal regions of the bithorax complex of Drosophila by gap genes. Development 121:1855–1866
Chell JM, Brand AH (2010) Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143:1161–1173
Chen F, Krasnow MA (2014) Progenitor outgrowth from the niche in Drosophila trachea is guided by FGF from decaying branches. Science 343:186–189
Cohen SM, Jürgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482–485
Cooley L, Theurkauf WE (1994) Cytoskeletal functions during Drosophila oogenesis. Science 266:590–596
Corty MM, Matthews BJ, Grueber WB (2009) Molecules and mechanisms of dendrite development in Drosophila. Development 136:1049–1061
Costa M, Wilson ET, Wieschaus E (1994) A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell 76:1075–1089
Crozatier M, Meister M (2007) Drosophila haematopoiesis. Cell Microbiol 9:1117–1126
Crozatier M, Ubeda JM, Vincent A, Meister M (2004) Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. PLoS Biol 2:E196
Dambly-Chaudière C, Jamet E, Burri M, Bopp D, Basler K, Hafen E, Dumont N, Spielmann P, Ghysen A, Noll M (1992) The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila. Cell 69:159–172
Dansereau DA, Lasko P (2008) The development of germline stem cells in Drosophila. Methods Mol Biol 450:3–26
Dawes-Hoang RE, Parmar KM, Christiansen AE, Phelps CB, Brand AH, Wieschaus EF (2005) Folded gastrulation, cell shape change and the control of myosin localization. Development 132(18):4165–4178
de Velasco B, Mandal L, Mkrtchyan M, Hartenstein V (2006) Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev Genes Evol 216:39–51
Denholm B, Hu N, Fauquier T, Caubit X, Fasano L, Skaer H (2013) The tiptop/teashirt genes regulate cell differentiation and renal physiology in Drosophila. Development 140:1100–1110
Deshpande G, Swanhart L, Chiang P, Schedl P (2001) Hedgehog signaling in germ cell migration. Cell 106:759–769
Dickson BJ, Gilestro GF (2006) Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 22:651–675
Di Cara F, King-Jones K (2013) How clocks and hormones act in concert to control the timing of insect development. Curr Top Dev Biol 105:1–36
DiNardo S, Sher E, Heemskerk-Jongens J, Kassis JA, O’Farrell PH (1988) Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis. Nature 332:604–609
DiNardo S, Heemskerk J, Dougan S, O’Farrell PH (1994) The making of a maggot: patterning the Drosophila embryonic epidermis. Curr Opin Genet Dev 4:529–534
Doe CQ, Technau GM (1993) Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci 16:510–514
Dubreuil RR (2004) Copper cells and stomach acid secretion in the Drosophila midgut. Int J Biochem Cell Biol 36:745–752
Dumstrei K, Wang F, Hartenstein V (2003) Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J Neurosci 23:3325–3335
Eastham LES (1930a) The formation of germ layers in insects. Biol Rev 5:1–29
Eastham LES (1930b) The embryology of Pieris rapae. Organogeny. Philos Trans R Soc Lond B 219:1–50
Ebens AJ, Garren H, Cheyette BN, Zipursky SL (1993) The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15–27
Edwards TN, Nuschke AC, Nern A, Meinertzhagen IA (2012) Organization and metamorphosis of glia in the Drosophila visual system. J Comp Neurol 520:2067–2085
Evans CJ, Hartenstein V, Banerjee U (2003) Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev Cell 5:673–690
Fernandes JJ, Celniker SE, VijayRaghavan K (1996) Development of the indirect flight muscle attachment sites in Drosophila: role of the PS integrins and the stripe gene. Dev Biol 176:166–184
Figeac N, Jagla T, Aradhya R, Da Ponte JP, Jagla K (2010) Drosophila adult muscle precursors form a network of interconnected cells and are specified by the rhomboid-triggered EGF pathway. Development 137:1965–1973
Fischbach KF, Hiesinger PR (2008) Optic lobe development. Adv Exp Med Biol 628:115–136
Fossett N, Tevosian SG, Gajewski K, Zhang Q, Orkin SH, Schulz RA (2001) The Friend of GATA proteins U-shaped, FOG-1, and FOG-2 function as negative regulators of blood, heart, and eye development in Drosophila. Proc Natl Acad Sci U S A 98:7342–7347
Fossett N, Hyman K, Gajewski K, Orkin SH, Schulz RA (2003) Combinatorial interactions of serpent, lozenge, and U-shaped regulate crystal cell lineage commitment during Drosophila hematopoiesis. Proc Natl Acad Sci U S A 100:11451–11456
Franke JD, Montague RA, Kiehart DP (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15:2208–2221
Frasch M (1999) Intersecting signalling and transcriptional pathways in Drosophila heart specification. Semin Cell Dev Biol 10:61–71
Fuller MT, Spradling AC (2007) Male and female Drosophila germline stem cells: two versions of immortality. Science 316:402–404
Fuss B, Hoch M (2002) Notch signaling controls cell fate specification along the dorsoventral axis of the Drosophila gut. Curr Biol 12:171–179
Fuss B, Josten F, Feix M, Hoch M (2004) Cell movements controlled by the Notch signalling cascade during foregut development in Drosophila. Development 131:1587–1595
García-Bellido A (1975) Genetic control of wing disc development in Drosophila. Ciba Found Symp 0:161–182
Gaul U, Jäckle H (1990) Role of gap genes in early Drosophila development. Adv Genet 27:239–275
Gaul U, Weigel D (1990) Regulation of Krüppel expression in the anlage of the Malpighian tubules in the Drosophila embryo. Mech Dev 33:57–67
Gehring WJ (1985–1986) Homeotic genes, the homeobox, and the spatial organization of the embryo. Harvey Lect 81:153–172
Gendre N, Lüer K, Friche S, Grillenzoni N, Ramaekers A, Technau GM, Stocker RF (2004) Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131:83–92
Ghysen A, Dambly-Chaudière C, Jan LY, Jan YN (1993) Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev 7:723–733
Gilbert SF (2006) Developmental biology, 8th edn. Sinauer Associates, Inc, Sunderland
Godt D, Laski FA (1995) Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric à brac. Development 121:173–187
Godt D, Tepass U (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395:387–391
Goodman CS, Doe CQ (1993) Embryonic development of the Drosophila central nervous system. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 941–1012
Goulding SE, zur Lage P, Jarman AP (2000) Amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 25:69–78
Grenningloh G, Goodman CS (1992) Pathway recognition by neuronal growth cones: genetic analysis of neural cell adhesion molecules in Drosophila. Curr Opin Neurobiol 2:42–47
Grigorian M, Mandal L, Hakimi M, Ortiz I, Hartenstein V (2011) The convergence of Notch and MAPK signaling specifies the blood progenitor fate in the Drosophila mesoderm. Dev Biol 353:105–118
Guha A, Kornberg TB (2005) Tracheal branch repopulation precedes induction of the Drosophila dorsal air sac primordium. Dev Biol 287:192–200
Guillemin K, Groppe J, Ducker K, Treisman R, Hafen E, Affolter M, Krasnow MA (1996) The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122:1353–1362
Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27–41
Hallberg E, Hansson BS (1999) Arthropod sensilla: morphology and phylogenetic considerations. Microsc Res Tech 47:428–439
Hanyu-Nakamura K, Kobayashi S, Nakamura A (2004) Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development 131:4545–4553
Harbecke R, Janning W (1989) The segmentation gene Krüppel of Drosophila melanogaster has homeotic properties. Genes Dev 3:114–122
Harding K, Wedeen C, McGinnis W, Levine M (1985) Spatially regulated expression of homeotic genes in Drosophila. Science 229:1236–1242
Hartenstein V (1997) Development of the insect stomatogastric nervous system. Trends Neurosci 20:421–427
Hartenstein V (2006) The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J Endocrinol 190:555–570
Hartenstein V (2011) Morphological diversity and development of glia in Drosophila. Glia 59:1237–1252
Hartenstein AY, Rugendorff A, Tepass U, Hartenstein V (1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116:1203–1220
Hartenstein V, Spindler S, Pereanu W, Fung S (2008) The development of the Drosophila larval brain. Adv Exp Med Biol 628:1–31
Hartmann B, Reichert H (1998) The genetics of embryonic brain development in Drosophila. Mol Cell Neurosci 12:194–205
Hayes SA, Miller JM, Hoshizaki DK (2001) Serpent, a GATA-like transcription factor gene, induces fat-cell development in Drosophila melanogaster. Development 128:1193–1200
Hoch M, Broadie K, Jäckle H, Skaer H (1994) Sequential fates in a single cell are established by the neurogenic cascade in the Malpighian tubules of Drosophila. Development 120:3439–3450
Hoch M, Pankratz MJ (1996) Control of gut development by fork head and cell signaling molecules in Drosophila. Mech Dev 58:3–14
Ingham PW (1991) Segment polarity genes and cell patterning within the Drosophila body segment. Curr Opin Genet Dev 1:261–267
Ip YT, Levine M, Small SJ (1992) The bicoid and dorsal morphogens use a similar strategy to make stripes in the Drosophila embryo. J Cell Sci Suppl 16:33–38
Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149:134–148
Jacinto A, Woolner S, Martin P (2002) Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev Cell 3:9–19
Jäckle H, Hoch M, Pankratz MJ, Gerwin N, Sauer F, Brönner G (1992) Transcriptional control by Drosophila gap genes. J Cell Sci Suppl 16:39–51
Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 23:125–133
Jan YN, Jan LY (1994) Genetic control of cell fate specification in Drosophila peripheral nervous system. Annu Rev Genet 28:373–393
Jarman AP, Groves AK (2013) The role of Atonal transcription factors in the development of mechanosensitive cells. Semin Cell Dev Biol 24:438–447
Jiang H, Edgar BA (2009) EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development 136:483–493
Jiang H, Grenley MO, Bravo MJ, Blumhagen RZ, Edgar BA (2011) EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 8:84–95
Jones BW (2005) Transcriptional control of glial cell development in Drosophila. Dev Biol 278:265–273
Jung AC, Denholm B, Skaer H, Affolter M (2005) Renal tubule development in Drosophila: a closer look at the cellular level. J Am Soc Nephrol 16:322–328
Jürgens G, Hartenstein V (1993) The terminal regions of the body patter. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 941–1012
Kaltschmidt JA, Brand AH (2002) Asymmetric cell division: microtubule dynamics and spindle asymmetry. J Cell Sci 115:2257–2264
Karpowicz P, Perez J, Perrimon N (2010) The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137:4135–4145
Kaufman TC, Seeger MA, Olsen G (1990) Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv Genet 27:309–362
Keshishian H, Chang TN, Jarecki J (1994) Precision and plasticity during Drosophila neuromuscular development. FASEB J 8:731–737
Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471–490
Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT (2001) Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294:2542–2545
King RC (1970) Ovarian development in Drosophila melanogaster. Academic, New York
Kirilly D, Xie T (2007) The Drosophila ovary: an active stem cell community. Cell Res 17:15–25. Erratum in: Cell Res 17:271
Klämbt C, Hummel T, Granderath S, Schimmelpfeng K (2001) Glial cell development in Drosophila. Int J Dev Neurosci 19:373–378
Klapper R (2000) The longitudinal visceral musculature of Drosophila melanogaster persists through metamorphosis. Mech Dev 95:47–54
Klapper R, Stute C, Schomaker O, Strasser T, Janning W, Renkawitz-Pohl R, Holz A (2002) The formation of syncytia within the visceral musculature of the Drosophila midgut is dependent on duf, sns and mbc. Mech Dev 110:85–96
Klingler M (1990) The organization of the antero-posterior axis. Semin Cell Biol 1:151–160
Kobayashi S, Okada M (1988) Molecular analysis of a cytoplasmic factor essential for pole cell formation in Drosophila embryos. Cell Differ Dev 25:25–29
Krzemień J, Dubois L, Makki R, Meister M, Vincent A, Crozatier M (2007) Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446:325–328
Krzemien J, Crozatier M, Vincent A (2010) Ontogeny of the Drosophila larval hematopoietic organ, hemocyte homeostasis and the dedicated cellular immune response to parasitism. Int J Dev Biol 54:1117–1125
Kuo YM, Jones N, Zhou B, Panzer S, Larson V, Beckendorf SK (1996) Salivary duct determination in Drosophila: roles of the EGF receptor signalling pathway and the transcription factors fork head and trachealess. Development 122:1909–1917
Lai EC, Orgogozo V (2004) A hidden program in Drosophila peripheral neurogenesis revealed: fundamental principles underlying sensory organ diversity. Dev Biol 269:1–17
Landgraf M, Sánchez-Soriano N, Technau GM, Urban J, Prokop A (2003) Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. Dev Biol 260:207–225
Larsen C, Shy D, Spindler SR, Fung S, Pereanu W, Younossi-Hartenstein A, Hartenstein V (2009) Patterns of growth, axonal extension and axonal arborization of neuronal lineages in the developing Drosophila brain. Dev Biol 335:289–304
Lawrence PA (1987) Pair-rule genes: do they paint stripes or draw lines? Cell 51:879–880
Lebestky T, Chang T, Hartenstein V, Banerjee U (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288:146–149
Lebestky T, Jung SH, Banerjee U (2003) A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev 17:348–353
Lee WC, Beebe K, Sudmeier L, Micchelli CA (2009) Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 136:2255–2264
Lehmann R, Nüsslein-Volhard C (1991) The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112:679–691
Lengyel JA, Iwaki DD (2002) It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev Biol 243:1–19
Leptin M (1995) Drosophila gastrulation: from pattern formation to morphogenesis. Annu Rev Cell Dev Biol 11:189–212
Levine M, Harding K (1987) Spatial regulation of homeo box gene expression in Drosophila. Oxf Surv Eukaryot Genes 4:116–142
Li MA, Alls JD, Avancini RM, Koo K, Godt D (2003) The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol 5:994–1000
Li X, Erclik T, Bertet C, Chen Z, Voutev R, Venkatesh S, Morante J, Celik A, Desplan C (2013) Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature 498:456–462
Lin G, Xu N, Xi R (2008) Paracrine wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455:1119–1123
Liu S, Jack J (1992) Regulatory interactions and role in cell type specification of the Malpighian tubules by the cut, Krüppel, and caudal genes of Drosophila. Dev Biol 150:133–143
Lo PC, Frasch M (2003) Establishing A-P polarity in the embryonic heart tube: a conserved function of Hox genes in Drosophila and vertebrates? Trends Cardiovasc Med 13:182–187
Lohmann I, McGinnis N, Bodmer M, McGinnis W (2002) The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110:457–466
Lu X, Perkins LA, Perrimon N (1993) The torso pathway in Drosophila: a model system to study receptor tyrosine kinase signal transduction. Dev Suppl 1993:47–56
Lubarsky B, Krasnow MA (2003) Tube morphogenesis: making and shaping biological tubes. Cell 112:19–28
Lucchetta EM, Ohlstein B (2012) The Drosophila midgut: a model for stem cell driven tissue regeneration. Wiley Interdiscip Rev Dev Biol 1:781–788
Mandal L, Dumstrei K, Hartenstein V (2004a) Role of FGFR signaling in the morphogenesis of the Drosophila visceral musculature. Dev Dyn 231:342–348
Mandal L, Banerjee U, Hartenstein V (2004b) Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat Genet 36:1019–1023
Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U (2007) A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 446:320–324
Manning G, Krasnow MA (1993) The development of the Drosophila tracheal system. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 941–1012
Manning AJ, Rogers SL (2014) The Fog signaling pathway: insights into signaling in morphogenesis. Dev Biol 394:6–14
Martin BS, Ruiz-Gómez M, Landgraf M, Bate M (2001) A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. Development 128:3331–3338
Martinez-Arias A, Lawrence PA (1985) Parasegments and compartments in the Drosophila embryo. Nature 313:639–642
Mathur D, Bost A, Driver I, Ohlstein B (2010) A transient niche regulates the specification of Drosophila intestinal stem cells. Science 327:210–213
Matsuzaki F (2000) Asymmetric division of Drosophila neural stem cells: a basis for neural diversity. Curr Opin Neurobiol 10:38–44
Meinertzhagen IA, Hanson TE (1993) Pattern formation in the Drosophila retina. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 1363–1492
Micchelli CA, Perrimon N (2006) Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439:475–479
Miller A (1950) The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 420–534
Mondal BC, Mukherjee T, Mandal L, Evans CJ, Sinenko SA, Martinez-Agosto JA, Banerjee U (2011) Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147:1589–1600
Morisato D, Anderson KV (1995) Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet 29:371–399
Moussian B, Roth S (2005) Dorsoventral axis formation in the Drosophila embryo–shaping and transducing a morphogen gradient. Curr Biol 15:R887–R899
Murakami R, Takashima S, Hamaguchi T (1999) Developmental genetics of the Drosophila gut: specification of primordia, subdivision and overt-differentiation. Cell Mol Biol (Noisy-le-Grand) 45:661–676
Murakami R, Okumura T, Uchiyama H (2005) GATA factors as key regulatory molecules in the development of Drosophila endoderm. Dev Growth Differ 47:581–589
Nassif C, Noveen A, Hartenstein V (2003) Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J Comp Neurol 455:417–434
Noselli S, Agnès F (1999) Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr Opin Genet Dev 9:466–472
Nüsslein-Volhard C (1991) Determination of the embryonic axes of Drosophila. Dev Suppl 1:1–10
Nüsslein-Volhard C, Roth S (1989) Axis determination in insect embryos. Ciba Found Symp 144:37–55
Oda H, Tsukita S, Takeichi M (1998) Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev Biol 203:435–450
Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474
Omoto JJ, Yogi P, Hartenstein V (2015) Origin and development of neuropil glia of the Drosophila larval and adult brain: two distinct glial populations derived from separate progenitors. Dev Biol (2015 Mar 14. pii: S0012-1606(15)00111-6). doi: 10.1016/j.ydbio.2015.03.004. [Epub ahead of print]
Panzer S, Weigel D, Beckendorf SK (1992) Organogenesis in Drosophila melanogaster: embryonic salivary gland determination is controlled by homeotic and dorsoventral patterning genes. Development 114:49–57
Park Y, Rangel C, Reynolds MM, Caldwell MC, Johns M, Nayak M, Welsh CJ, McDermott S, Datta S (2003) Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev Biol 253:247–257
Parks S, Wieschaus E (1991) The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell 64:447–458
Pearson BJ, Doe CQ (2004) Specification of temporal identity in the developing nervous system. Annu Rev Cell Dev Biol 20:619–647
Pereanu W, Shy D, Hartenstein V (2005) Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191–203
Pereanu W, Kumar A, Jennett A, Reichert H, Hartenstein V (2010) Development-based compartmentalization of the Drosophila central brain. J Comp Neurol 518:2996–3023
Pitsouli C, Perrimon N (2010) Embryonic multipotent progenitors remodel the Drosophila airways during metamorphosis. Development 137:3615–3624
Prokop A, Bray S, Harrison E, Technau GM (1998) Homeotic regulation of segment-specific differences in neuroblast numbers and proliferation in the Drosophila central nervous system. Mech Dev 74:99–110
Rajagopalan S, Vivancos V, Nicolas E, Dickson BJ (2000) Selecting a longitudinal pathway: robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103:1033–1045
Ready DF, Hanson TE, Benzer S (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240
Rehorn KP, Thelen H, Michelson AM, Reuter R (1996) A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development 122:4023–4031
Ren F, Wang B, Yue T, Yun EY, Ip YT, Jiang J (2010) Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci U S A 107:21064–210649
Riechmann V, Irion U, Wilson R, Grosskortenhaus R, Leptin M (1997) Control of cell fates and segmentation in the Drosophila mesoderm. Development 124:2915–2922
Riechmann V, Rehorn KP, Reuter R, Leptin M (1998) The genetic control of the distinction between fat body and gonadal mesoderm in Drosophila. Development 125:713–723
Riley PD, Carroll SB, Scott MP (1987) The expression and regulation of Sex combs reduced protein in Drosophila embryos. Genes Dev 1:716–730
Rivera-Pomar R, Lu X, Perrimon N, Taubert H, Jäckle H (1995) Activation of posterior gap gene expression in the Drosophila blastoderm. Nature 376:253–256
Rizki TM (1980) The circulatory system and associated cells and tissues. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2b. Academic, London
Rochlin K, Yu S, Roy S, Baylies MK (2010) Myoblast fusion: when it takes more to make one. Dev Biol 341:66–83
Roy S, VijayRaghavan K (1997) Homeotic genes and the regulation of myoblast migration, fusion and fibre-specific gene expression during adult myogenesis in Drosophila. Development 124:3333–3341
Roy S, VijayRaghavan K (1999) Muscle pattern diversification in Drosophila: the story of imaginal myogenesis. Bioessays 21:486–498
Roy S, Shashidhara LS, VijayRaghavan K (1997) Muscles in the Drosophila second thoracic segment are patterned independently of autonomous homeotic gene function. Curr Biol 7:222–227
Rugendorff AE, Younossi-Hartenstein A, Hartenstein V (1993) Embryonic development of the Drosophila heart. Roux’s Arch Dev Biol 203:266–280
Ruohola-Baker H, Jan LY, Jan YN (1994) The role of gene cassettes in axis formation during Drosophila oogenesis. Trends Genet 10:89–94
Rusch J, Levine M (1996) Threshold responses to the dorsal regulatory gradient and the subdivision of primary tissue territories in the Drosophila embryo. Curr Opin Genet Dev 6:416–423
Rushlow C, Arora K (1990) Dorsal-ventral polarity and pattern formation in the Drosophila embryo. Semin Cell Biol 1:137–149
Samakovlis C, Manning G, Steneberg P, Hacohen N, Cantera R, Krasnow MA (1996) Genetic control of epithelial tube fusion during Drosophila tracheal development. Development 122:3531–3536
Sato M, Kornberg TB (2002) FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev Cell 3:195–207
Sato M, Suzuki T, Nakai Y (2013) Waves of differentiation in the fly visual system. Dev Biol 380:1–11
Schottenfeld J, Song Y, Ghabrial AS (2010) Tube continued: morphogenesis of the Drosophila tracheal system. Curr Opin Cell Biol 22:633–639
Schulz RA, Fossett N (2005) Hemocyte development during Drosophila embryogenesis. Methods Mol Med 105:109–122
Schulz C, Tautz D (1995) Zygotic caudal regulation by hunchback and its role in abdominal segment formation of the Drosophila embryo. Development 121:1023–1028
Schüpbach T, Roth S (1994) Dorsoventral patterning in Drosophila oogenesis. Curr Opin Genet Dev 4:502–507
Schweisguth F, Vincent A, Lepesant JA (1991) Genetic analysis of the cellularization of the Drosophila embryo. Biol Cell 72:15–23
Schweitzer R, Zelzer E, Volk T (2010) Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates. Development 137:2807–2817. Erratum in: development (2010) 137:3347
Shanbhag S, Tripathi S (2009) Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J Exp Biol 212:1731–1744
Shaw RL, Kohlmaier A, Polesello C, Veelken C, Edgar BA, Tapon N (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137:4147–4158
Shim J, Mukherjee T, Banerjee U (2012) Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol 14:394–400
Siegmund T, Korge G (2001) Innervation of the ring gland of Drosophila melanogaster. J Comp Neurol 431:481–491
Sinenko SA, Mandal L, Martinez-Agosto JA, Banerjee U (2009) Dual role of wingless signaling in stem-like hematopoietic precursor maintenance in Drosophila. Dev Cell 16:756–763
Singh SR, Liu W, Hou SX (2007) The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 1:191–203
Singh SR, Zeng X, Zheng Z, Hou SX (2011) The adult Drosophila gastric and stomach organs are maintained by a multipotent stem cell pool at the foregut/midgut junction in the cardia (proventriculus). Cell Cycle 10:1109–1120
Skaer H (1993) The alimentary canal. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 941–1012
Skeath JB, Carroll SB (1994) The achaete-scute complex: generation of cellular pattern and fate within the Drosophila nervous system. FASEB J 8:714–721
Skeath JB, Thor S (2003) Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 13:8–15
Small S, Levine M (1991) The initiation of pair-rule stripes in the Drosophila blastoderm. Curr Opin Genet Dev 1:255–260
Søndergaard L (1993) Homology between the mammalian liver and the Drosophila fat body. Trends Genet 9:193
Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508–512
Soustelle L, Giangrande A (2007) Glial differentiation and the Gcm pathway. Neuron Glia Biol 3:5–16
Spindler SR, Hartenstein V (2010) The Drosophila neural lineages: a model system to study brain development and circuitry. Dev Genes Evol 220:1–10
Spradling A, Fuller MT, Braun RE, Yoshida S (2011) Germline stem cells. Cold Spring Harb Perspect Biol 3:a002642
Staehling-Hampton K, Hoffmann FM, Baylies MK, Rushton E, Bate M (1994) Dpp induces mesodermal gene expression in Drosophila. Nature 372:783–786
Stanojevi D, Hoey T, Levine M (1989) Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature 341:331–335
Stork T, Bernardos R, Freeman MR (2012) Analysis of glial cell development and function in Drosophila. Cold Spring Harb Protoc 2012:1–17
Stork T, Sheehan A, Tasdemir-Yilmaz OE, Freeman MR (2014) Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes. Neuron 83:388–403
Takashima S, Hartenstein V (2012) Genetic control of intestinal stem cell specification and development: a comparative view. Stem Cell Rev 8:597–608
Takashima S, Mkrtchyan M, Younossi-Hartenstein A, Merriam JR, Hartenstein V (2008) The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signalling. Nature 454:651–655
Takashima S, Adams KL, Ortiz PA, Ying CT, Moridzadeh R, Younossi-Hartenstein A, Hartenstein V (2011a) Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway. Dev Biol 353:161–172
Takashima S, Younossi-Hartenstein A, Ortiz PA, Hartenstein V (2011b) A novel tissue in an established model system: the Drosophila pupal midgut. Dev Genes Evol 221:69–81
Takashima S, Paul M, Aghajanian P, Younossi-Hartenstein A, Hartenstein V (2013) Migration of Drosophila intestinal stem cells across organ boundaries. Development 140:1903–1911
Takashima S, Aghajanian P, Younossi-Hartenstein A, Paul M, Hartenstein V (2014) Origin and dynamic lineage characteristics of the developing Drosophila midgut stem cells (in review)
Tasdemir-Yilmaz OE, Freeman MR (2014) Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev 28:20–33
Tepass U, Hartenstein V (1994a) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563–596
Tepass U, Hartenstein V (1994b) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120:579–590
Tepass U, Hartenstein V (1995) Neurogenic and proneural genes control cell fate specification in the Drosophila endoderm. Development 121:393–405
Tepass U, Fessler LI, Aziz A, Hartenstein V (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120:1829–1837
Tilney LG, DeRosier DJ (2005) How to make a curved Drosophila bristle using straight actin bundles. Proc Natl Acad Sci U S A 102:18785–18792
Tixier V, Bataillé L, Jagla K (2010) Diversification of muscle types: recent insights from Drosophila. Exp Cell Res 316:3019–3027
Tomancak P, Beaton A, Weiszmann R, Kwan E, Shu S, Lewis SE, Richards S, Ashburner M, Hartenstein V, Celniker SE, Rubin GM (2002) Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol 3:research0088.1
Treisman JE (2013) Retinal differentiation in Drosophila. Wiley Interdiscip Rev Dev Biol 2:545–557
Truman JW, Moats W, Altman J, Marin EC, Williams DW (2010) Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. Development 137:53–61
Tulina N, Matunis E (2001) Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294:2546–2549
Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN (1989) numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58:349–360
VanHook A, Letsou A (2008) Head involution in Drosophila: genetic and morphogenetic connections to dorsal closure. Dev Dyn 237:28–38
Viktorin G, Riebli N, Popkova A, Giangrande A, Reichert H (2011) Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev Biol 356:553–565
Volk T (1999) Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet 15:448–453
von Ohlen T, Doe CQ (2000) Convergence of dorsal, dpp, and egfr signaling pathways subdivides the Drosophila neuroectoderm into three dorsal-ventral columns. Dev Biol 224:362–372
Wang S, Tulina N, Carlin DL, Rulifson EJ (2007) The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proc Natl Acad Sci U S A 104:19873–19878
Ward EJ, Skeath JB (2000) Characterization of a novel subset of cardiac cells and their progenitors in the Drosophila embryo. Development 127:4959–4969
Warn RM, Warn A, Planques V, Robert-Nicoud M (1990) Cytokinesis in the early Drosophila embryo. Ann N Y Acad Sci 582:222–232
Warrior R (1994) Primordial germ cell migration and the assembly of the Drosophila embryonic gonad. Dev Biol 166:180–194
Weavers H, Prieto-Sánchez S, Grawe F, Garcia-López A, Artero R, Wilsch-Bräuninger M, Ruiz-Gómez M, Skaer H, Denholm B (2009) The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature 457:322–326
Wernet MF, Desplan C (2004) Building a retinal mosaic: cell-fate decision in the fly eye. Trends Cell Biol 14:576–584
White RA, Lehmann R (1986) A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47:311–321
Williams DW, Shepherd D (2002) Persistent larval sensory neurones are required for the normal development of the adult sensory afferent projections in Drosophila. Development 129:617–624
Wilson R, Leptin M (2000) Fibroblast growth factor receptor-dependent morphogenesis of the Drosophila mesoderm. Philos Trans R Soc Lond B Biol Sci 355:891–895
Wodarz A (2005) Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Curr Opin Cell Biol 17:475–481
Wolff T, Ready DF (1993) Pattern formation in the Drosophila retina. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Habor Laboratory Press, Plainview, pp 1277–1326
Wolpert L (1989) Positional information revisited. Development 107:3–12
Wolpert L (2002) Principles of development, 2nd edn. Oxford University Press, Oxford
Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290:328–330
Xu N, Wang SQ, Tan D, Gao Y, Lin G, Xi R (2011) EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev Biol 354:31–43
Yu HH, Kolodkin AL (1999) Semaphorin signaling: a little less per-plexin. Neuron 22:11–14
Yu F, Kuo CT, Jan YN (2006) Drosophila neuroblast asymmetric cell division: recent advances and implications for stem cell biology. Neuron 51:13–20
Zamore PD, Lehmann R (1996) Drosophila development: homeodomains and translational control. Curr Biol 6:773–775
Zhuang S, Shao H, Guo F, Trimble R, Pearce E, Abmayr SM (2009) Sns and Kirre, the Drosophila orthologs of Nephrin and Neph1, direct adhesion, fusion and formation of a slit diaphragm-like structure in insect nephrocytes. Development 136:2335–2344
Zlatic M, Landgraf M, Bate M (2003) Genetic specification of axonal arbors: atonal regulates robo3 to position terminal branches in the Drosophila nervous system. Neuron 37:41–51
Zlatic M, Li F, Strigini M, Grueber W, Bate M (2009) Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis. PLoS Biol 7:e1000135
Acknowledgments
VH wrote most of the text of this chapter and prepared the figures. He warmly thanks ADC for writing the introductory sections and contributing to other sections.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer-Verlag Wien
About this chapter
Cite this chapter
Hartenstein, V., Chipman, A.D. (2015). Hexapoda: A Drosophila’s View of Development. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 5. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1868-9_1
Download citation
DOI: https://doi.org/10.1007/978-3-7091-1868-9_1
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-1867-2
Online ISBN: 978-3-7091-1868-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)