1932

Abstract

The developmental mechanisms that control body size and the relative sizes of body parts are today best understood in insects. Size is controlled by the mechanisms that cause growth to stop when a size characteristic of the species has been achieved. This requires the mechanisms to assess size and respond by stopping the process that controls growth. Growth is controlled by two hormones, insulin and ecdysone, that act synergistically by controlling cell growth and cell division. Ecdysone has two distinct functions: At low concentration it controls growth, and at high levels it causes molting and tissue differentiation. Growth is stopped by the pulse of ecdysone that initiates the metamorphic molt. Body size is sensed by either stretch receptors or oxygen restriction, depending on the species, which stimulate the high level of ecdysone secretion that induces a molt. Wing growth occurs mostly after the body has stopped growing. Wing size is adjusted to body size by variation in both the duration and level of ecdysone secretion.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-010814-020841
2015-01-07
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/ento/60/1/annurev-ento-010814-020841.html?itemId=/content/journals/10.1146/annurev-ento-010814-020841&mimeType=html&fmt=ahah

Literature Cited

  1. Agui N. 1.  1973. Quantitative bioassay of moulting hormone in vitro. Appl. Entomol. Zool. 8:236–39 [Google Scholar]
  2. Azevedo RBR, French V, Partridge L. 2.  2002. Temperature modulates epidermal cell size in Drosophila melanogaster. J. Insect Physiol. 48:231–37 [Google Scholar]
  3. Baker F, Tsai LW, Reuter C, Schooley D. 3.  1987. In vivo fluctuation of JH, JH acid, and ecdysteroid titer, and JH esterase activity, during development of fifth stadium Manduca sexta. Insect Biochem. 17:989–96 [Google Scholar]
  4. Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA. 4.  2002. Drosophila's insulin/P13-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2:239–49 [Google Scholar]
  5. Browder MH, D'Amico LJ, Nijhout HF. 5.  2001. The role of low levels of juvenile hormone esterase in the metamorphosis of Manduca sexta. J. Insect Sci. 1:11 [Google Scholar]
  6. Callier V, Nijhout HF. 6.  2011. Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc. Natl. Acad. Sci. USA 108:14664–69 [Google Scholar]
  7. Callier V, Nijhout HF. 7.  2013. Body size determination in insects: a review and synthesis of size- and brain-dependent and independent mechanisms. Biol. Rev. 88:944–54 [Google Scholar]
  8. Champlin DT, Truman JW. 8.  1998. Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta. Development 125:2009–18 [Google Scholar]
  9. Chapman RF. 9.  1998. The Insects: Structure and Function Cambridge: Cambridge Univ. Press
  10. Cherbas L, Willingham A, Zhang D, Yang L, Zou Y. 10.  et al. 2011. The transcriptional diversity of 25 Drosophila cell lines. Genome Res. 21:301–14 [Google Scholar]
  11. Chiang RG, Davey KG. 11.  1988. A novel receptor capable of monitoring applied pressure in the abdomen of an insect. Science 241:1665–67 [Google Scholar]
  12. Cole B. 12.  1980. Growth ratios in holometabolous and hemimetabolous insects. Ann. Entomol. Soc. Am. 79:489–91 [Google Scholar]
  13. Colombani J, Andersen DS, Léopold P. 13.  2012. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336:582–85 [Google Scholar]
  14. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. 14.  2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114:739–49 [Google Scholar]
  15. Davidowitz G, D'Amico LJ, Nijhout HF. 15.  2004. The effects of environmental variation on a mechanism that controls insect body size. Evol. Ecol. Res. 6:49–62 [Google Scholar]
  16. Dyar H. 16.  1890. The number of molts of lepidopterous larvae. Psyche 5:420–22 [Google Scholar]
  17. Eberhard WG, Wcislo WT. 17.  2011. Morphological and behavioral consequences of physiological limitations in miniature arthropods. Adv. Insect Physiol. 40:155–214 [Google Scholar]
  18. Eberhard WG, Wcislo WT. 18.  2012. Plenty of room at the bottom? Tiny animals solve problems of housing and maintaining oversized brains, shedding new light on nervous-system evolution. Am. Sci. 100:226–33 [Google Scholar]
  19. Edgar BA, Orr-Weaver TL. 19.  2001. Endoreplication cell cycles: more for less. Cell 105:297–306 [Google Scholar]
  20. Esperk T, Tammaru T, Nylin S. 20.  2007. Intraspecific variability in number of larval instars in insects. J. Econ. Entomol. 100:627–45 [Google Scholar]
  21. Fain MJ, Riddiford LM. 21.  1975. Juvenile hormone titers in the hemolymph during late larval development of the tobacco hornworm, Manduca sexta (L.). Biol. Bull. 149:506–21 [Google Scholar]
  22. Fain MJ, Riddiford LM. 22.  1977. Requirements for molting of the crochet epidermis of the tobacco hornworm larva in vivo and in vitro. Wilhelm Roux' Arch. 181:285–307 [Google Scholar]
  23. Furuta K, Ichikawa A, Murata M, Kuwano E, Shinoda T, Shiotsuki T. 23.  2013. Determination by LC-MS of juvenile hormone titers in hemolymph of the silkworm, Bombyx mori. Biosci. Biotechnol. Biochem. 77:988–91 [Google Scholar]
  24. Greenlee KJ, Harrison JF. 24.  2005. Respiratory changes throughout ontogeny in the tobacco hornworm caterpillar, Manduca sexta. J. Exp. Biol. 208:1385–92 [Google Scholar]
  25. Hakim RS, Baldwin K, Smagghe G. 25.  2010. Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Entomol. 55:593–608 [Google Scholar]
  26. Hammock BD. 26.  1985. Regulation of juvenile hormone titer: degradation. Comprehensive Insect Physiology, Biochemistry, and Pharmacology GA Kerkut, LI Gilbert 431–72 New York: Pergamon [Google Scholar]
  27. Harrison JF, Frazier MR, Henry JR, Kaiser A, Klok CJ, Rascon B. 27.  2006. Responses of terrestrial insects to hypoxia or hyperoxia. Respir. Physiol. Neurobiol. 154:4–17 [Google Scholar]
  28. Harrison JF, Haddad GG. 28.  2011. Effects of oxygen on growth and size: synthesis of molecular, organismal, and evolutionary studies with Drosophila melanogaster. Annu. Rev. Physiol. 73:95–113 [Google Scholar]
  29. Harrison JF, Kaiser A, VandenBrooks JM. 29.  2010. Atmospheric oxygen level and the evolution of insect body size. Proc. R. Soc. B 277:1937–46 [Google Scholar]
  30. Heinrich EC, Farzin M, Klok CJ, Harrison JF. 30.  2011. The effect of developmental stage on the sensitivity of cell and body size to hypoxia in Drosophila melanogaster. J. Exp. Biol. 214:1419–27 [Google Scholar]
  31. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E. 31.  2002. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12:1293–300 [Google Scholar]
  32. Jones HN, Ashworth CJ, Page KR, McArdle HJ. 32.  2006. Expression and adaptive regulation of amino acid transport system A in a placental cell line under amino acid restriction. Reproduction 131:951–60 [Google Scholar]
  33. Kato Y, Nair KK, Dyer KA, Riddiford LM. 33.  1987. Changes in ploidy level of epidermal cells during last larval instar of the tobacco hornworm, Manduca sexta. Development 99:137–43 [Google Scholar]
  34. Kato Y, Riddiford L. 34.  1987. The role of 20-hydroxyecdysone in stimulating epidermal mitoses during the larval-pupal transformation of the tobacco hornworm, Manduca sexta. Development 100:227–36 [Google Scholar]
  35. Kilberg M. 35.  1982. Amino acid transport in isolated rat hepatocytes. J. Membr. Biol. 69:1–12 [Google Scholar]
  36. Kim SK, Rulifson EJ. 36.  2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:316–20 [Google Scholar]
  37. Kingsolver JG. 37.  2007. Variation in growth and instar number in field and laboratory Manduca sexta. Proc. R. Soc. B 274:977–81 [Google Scholar]
  38. Klingenberg CP, Nijhout HF. 38.  1998. Competition among growing organs and developmental control of morphological asymmetry. Proc. R. Soc. Lond. B 265:1135–39 [Google Scholar]
  39. Koyama T, Obara Y, Iwami M, Sakurai S. 39.  2004. Commencement of pupal commitment in late penultimate instar and its hormonal control in wing imaginal discs of the silkworm, Bombyx mori. J. Insect Physiol. 50:123–33 [Google Scholar]
  40. Kremen C, Nijhout HF. 40.  1989. Juvenile hormone controls the onset of pupal commitment in the imaginal disks and epidermis of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 35:603–12 [Google Scholar]
  41. Kremen C, Nijhout HF. 41.  1998. Control of pupal commitment in the imaginal disks of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 44:287–96 [Google Scholar]
  42. Layalle S, Arquier N, Léopold P. 42.  2008. The TOR pathway couples nutrition and developmental timing in Drosophila. Dev. Cell 15:568–77 [Google Scholar]
  43. Leopold P, Layalle S. 43.  2006. Linking nutrition and tissue growth. Science 312:1317–18 [Google Scholar]
  44. Lynn DE. 44.  2002. Methods for maintaining insect cell cultures. J. Insect Sci. 2:9 [Google Scholar]
  45. Makarova AA, Polilov AA. 45.  2013. Peculiarities of the brain organization and fine structure in small insects related to miniaturization. 1. The smallest Coleoptera (Ptiliidae). Entomol. Rev. 93:703–13 [Google Scholar]
  46. Maramorosch K. 46.  1976. Invertebrate Tissue Culture Research Applications New York: Academic
  47. Marks EP. 47.  1972. Effects of ecdysterone on the deposition of cockroach cuticle in vitro. Biol. Bull. 142:293–301 [Google Scholar]
  48. Marks EP. 48.  1980. Insect tissue culture: an overview, 1971–1978. Annu. Rev. Entomol. 25:73–101 [Google Scholar]
  49. Masumura M, Satake SI, Saegusa H, Mizoguchi A. 49.  2000. Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. Gen. Comp. Endocrinol. 118:393–99 [Google Scholar]
  50. McCabe J, French V, Partridge L. 50.  1997. Joint regulation of cell size and cell number in the wing blade of Drosophila melanogaster. Genet. Res. 69:61–68 [Google Scholar]
  51. McDowell HE, Eyers PA, Hundal HS. 51.  1998. Regulation of System A amino acid transport in L6 rat skeletal muscle cells by insulin, chemical and hyperthermic stress. FEBS Lett. 441:15–19 [Google Scholar]
  52. Minelli A, Maruzzo D, Fusco G. 52.  2010. Multi-scale relationships between numbers and size in the evolution of arthropod body features. Arthropod Struct. Dev. 39:468–77 [Google Scholar]
  53. Mirth C, Truman JW, Riddiford LM. 53.  2005. The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr. Biol. 15:1796–807 [Google Scholar]
  54. Mirth CK, Riddiford LM. 54.  2007. Size assessment and growth control: how adult size is determined in insects. Bioessays 29:344–55 [Google Scholar]
  55. Mitsuhashi J, Inoue H. 55.  1988. Obtainment of a continuous cell line from the larval fat bodies of the mulberry tiger moth, Spilosoma imparilis (Lepidoptera: Arctiidae). Appl. Entomol. Zool. 23:488–90 [Google Scholar]
  56. Mizoguchi A, Hatta M, Sato S, Nagasawa H, Suzuki A, Ishizaki H. 56.  1990. Developmental change of bombyxin content in the brain of the silkmoth Bombyx mori. J. Insect Physiol. 36:655–59 [Google Scholar]
  57. Niimi S, Sakurai S. 57.  1997. Development changes in juvenile hormone and juvenile hormone acid titers in the hemolymph and in-vitro juvenile hormone synthesis by corpora allata of the silkworm, Bombyx mori. J. Insect Physiol. 43:875–84 [Google Scholar]
  58. Nijhout HF. 58.  1975. A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta (L.). Biol. Bull. 149:214–25 [Google Scholar]
  59. Nijhout HF. 59.  1975. Axonal pathways in the brain-retrocerebral neuroendocrine complex of Manduca sexta (L.) (Lepidoptera: Sphingidae). Int. J. Insect Morphol. Embryol. 4:529–38 [Google Scholar]
  60. Nijhout HF. 60.  1979. Stretch-induced moulting in Oncopeltus fasciatus. J. Insect Physiol. 25:277–82 [Google Scholar]
  61. Nijhout HF. 61.  1984. Abdominal stretch reception in Dipetalogaster maximus (Hemiptera: Reduviidae). J. Insect Physiol. 30:629–33 [Google Scholar]
  62. Nijhout HF. 62.  1994. Insect Hormones Princeton, NJ: Princeton Univ. Press
  63. Nijhout HF. 63.  2002. The control of body size in Manduca sexta. Dev. Biol. 247:483 (Abstr.) [Google Scholar]
  64. Nijhout HF. 64.  2003. The control of body size in insects. Dev. Biol. 261:1–9 [Google Scholar]
  65. Nijhout HF, Davidowitz G, Roff DA. 65.  2006. A quantitative analysis of the mechanism that controls body size in Manduca sexta. J. Biol. 5:16 [Google Scholar]
  66. Nijhout HF, Emlen DJ. 66.  1998. Competition among body parts in the development and evolution of insect morphology. Proc. Natl. Acad. Sci. USA 95:3685–89 [Google Scholar]
  67. Nijhout HF, Grunert LW. 67.  2002. Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc. Natl. Acad. Sci. USA 99:15446–50 [Google Scholar]
  68. Nijhout HF, Grunert LW. 68.  2010. The cellular and physiological mechanism of wing-body scaling in Manduca sexta. Science 330:1693–95 [Google Scholar]
  69. Nijhout HF, Riddiford LM, Mirth C, Shingleton AW, Suzuki Y, Callier V. 69.  2014. The developmental control of size in insects. Wiley Interdiscipl. Rev. Dev. Biol. 3:113–34 [Google Scholar]
  70. Nijhout HF, Smith WA, Schachar I, Subramanian S, Tobler A, Grunert LW. 70.  2007. The control of growth and differentiation of the wing imaginal disks of Manduca sexta. Dev. Biol. 302:569–76 [Google Scholar]
  71. Nijhout HF, Williams CM. 71.  1974. Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): cessation of juvenile hormone secretion as a trigger for pupation. J. Exp. Biol. 61:493–501 [Google Scholar]
  72. Niven JE, Farris SM. 72.  2012. Miniaturization of nervous systems and neurons. Curr. Biol. 22:R323–29 [Google Scholar]
  73. Okamoto N, Yamanaka N, Satake H, Saegusa H, Kataoka H, Mizoguchi A. 73.  2009. An ecdysteroid-inducible insulin-like growth factor-like peptide regulates adult development of the silkmoth Bombyx mori. FEBS J. 276:1221–32 [Google Scholar]
  74. Okamoto N, Yamanaka N, Yagi Y, Nishida Y, Kataoka H. 74.  et al. 2009. A fat body-derived IGF-like peptide regulates postfeeding growth in Drosophila. Dev. Cell 17:885–91 [Google Scholar]
  75. Parker NF, Shingleton AW. 75.  2011. The coordination of growth among Drosophila organs in response to localized growth-perturbation. Dev. Biol. 357:318–25 [Google Scholar]
  76. Partridge L, Barrie B, Fowler K, French V. 76.  1994. Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48:1269–76 [Google Scholar]
  77. Polilov AA. 77.  2008. Anatomy of the smallest coleoptera, featherwing beetles of the tribe Nanosellini (Coleoptera, Ptiliidae), and limits of insect miniaturization. Entomol. Rev. 88:26–33 [Google Scholar]
  78. Polilov AA. 78.  2012. The smallest insects evolve anucleate neurons. Arthropod Struct. Dev. 41:29–34 [Google Scholar]
  79. Polilov AA, Beutel RG. 79.  2009. Miniaturisation effects in larvae and adults of Mikado sp. (Coleoptera: Ptiliidae), one of the smallest free-living insects. Arthropod Struct. Dev. 38:247–70 [Google Scholar]
  80. Quinn L, Lin J, Cranna N, Lee JEA, Mitchell N, Hannan R. 80.  2012. Steroid hormones in Drosophila: how ecdysone coordinates developmental signalling with cell growth and division. Steroids—Basic Science H Abduljabbar 141–68 Rijeka, Croat: InTech [Google Scholar]
  81. Raikhel A, Deitsch K, Sappington T. 81.  1997. Culture and analysis of the insect fat body. The Molecular Biology of Insect Disease Vectors J Crampton, CB Beard, C Louis 507–22 London: Chapman Hall [Google Scholar]
  82. Rensch B. 82.  1948. Histological changes correlated with evolutionary changes of body size. Evolution 2:218–30 [Google Scholar]
  83. Riddiford LM. 83.  1976. Hormonal control of insect epidermal cell commitment in vitro. Nature 259:115–17 [Google Scholar]
  84. Riddiford LM. 84.  1978. Ecdysone-induced change in cellular commitment of the epidermis of the tobacco hornworm, Manduca sexta, at the initiation of metamorphosis. Gen. Comp. Endocrinol. 34:438–46 [Google Scholar]
  85. Roberts B, Gilbert LI, Bollenbacher WE. 85.  1984. In vitro activity of dipteran ring glands and activation by the prothoracicotropic hormone. Gen. Comp. Endocrinol. 54:469–77 [Google Scholar]
  86. Rountree D, Bollenbacher W. 86.  1986. The release of the prothoracicotropic hormone in the tobacco hornworm, Manduca sexta, is controlled intrinsically by juvenile hormone. J. Exp. Biol. 120:41–58 [Google Scholar]
  87. Rulifson EJ, Kim SK, Nusse R. 87.  2002. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–20 [Google Scholar]
  88. Saegusa H, Mizoguchi A, Kitahora H, Nagasawa H, Suzuki A, Ishizaki H. 88.  1992. Changes in the titer of bombyxin-immunoreactive material in hemolymph during the postembryonic development of the silkmoth Bombyx mori. Dev. Growth Differ. 34:595–605 [Google Scholar]
  89. Schweitzer R, Shilo B-Z. 89.  1997. A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13:191–96 [Google Scholar]
  90. Shafiei M, Moczek AP, Nijhout HF. 90.  2001. Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiol. Entomol. 26:173–80 [Google Scholar]
  91. Shingleton AW, Das J, Vinicius L, Stern D. 91.  2005. The temporal requirements for insulin signaling during development in Drosophila. PLOS Biol. 3:e289 [Google Scholar]
  92. 92.  Deleted in proof
  93. Slaidina M, Delanoue R, Gronke S, Partridge L, Léopold P. 93.  2009. A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev. Cell 17:874–84 [Google Scholar]
  94. Smagghe GUY, Vanhassel W, Moeremans C, De Wilde D, Goto S. 94.  et al. 2005. Stimulation of midgut stem cell proliferation and differentiation by insect hormones and peptides. Ann. N. Y. Acad. Sci. 1040:472–75 [Google Scholar]
  95. Sparks TC, Hammock BD, Riddiford LM. 95.  1983. The hemolymph juvenile-hormone esterase of Manduca sexta (L)—inhibition and regulation. Insect Biochem. 13:529–41 [Google Scholar]
  96. Stieper BC, Kupershtok M, Driscoll MV, Shingleton AW. 96.  2008. Imaginal discs regulate developmental timing in Drosophila melanogaster. Dev. Biol. 321:18–26 [Google Scholar]
  97. Struhl G, Barbash DA, Lawrence PA. 97.  1997. Hedgehog organises the pattern and polarity of epidermal cells in the Drosophila abdomen. Development 124:2143–54 [Google Scholar]
  98. Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shingleton AW. 98.  2011. FOXO regulates organ-specific phenotypic plasticity in Drosophila. PLOS Genet. 7:e1002373 [Google Scholar]
  99. Tobler A, Nijhout HF. 99.  2010. A switch in the control of growth of the wing imaginal disks of Manduca sexta. PLOS ONE 5:e10723 [Google Scholar]
  100. Truman JW. 100.  1972. Physiology of insect rhythms. I. Circadian organization of the endocrine events underlying the moulting cycle of larval tobacco hornworms. J. Exp. Biol. 57:805–20 [Google Scholar]
  101. Truman JW, Riddiford LM. 101.  1974. Physiology of insect rhythms. III. The temporal organization of the endocrine events underlying pupation of the tobacco hornworm. J. Exp. Biol. 60:371–82 [Google Scholar]
  102. Vago C. 102.  1971. Invertebrate Tissue Culture New York: Academic
  103. Walkiewicz MA, Stern M. 103.  2009. Increased insulin/insulin growth factor signaling advances the onset of metamorphosis in Drosophila. PLOS ONE 4:e5072 [Google Scholar]
  104. Weinkove D, Neufeld TP, Twardzik T, Waterfield MD, Leevers SJ. 104.  1999. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class IA phosphoinositide 3-kinase and its adaptor. Curr. Biol. 9:1019–29 [Google Scholar]
  105. Weis-Fogh T. 105.  1964. Diffusion in insect wing muscle, the most active tissue known. J. Exp. Biol. 41:229–56 [Google Scholar]
  106. Williams C. 106.  1980. Growth in insects. Insect Biology in the Future M Locke, DS Smith 369–83 New York: Academic [Google Scholar]
  107. Wolfgang W, Riddiford L. 107.  1981. Cuticular morphogenesis during continuous growth of the final instar larva of a moth. Tissue Cell 13:757–72 [Google Scholar]
  108. Wolfgang W, Riddiford L. 108.  1986. Larval cuticular morphogenesis in the tobacco hornworm, Manduca sexta, and its hormonal regulation. Dev. Biol. 113:305–16 [Google Scholar]
/content/journals/10.1146/annurev-ento-010814-020841
Loading
/content/journals/10.1146/annurev-ento-010814-020841
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error