1932

Abstract

All organisms are exposed to changes in their environment throughout their life cycle. When confronted with these changes, they adjust their development and physiology to ensure that they can produce the functional structures necessary for survival and reproduction. While some traits are remarkably invariant, or robust, across environmental conditions, others show high degrees of variation, known as plasticity. Generally, developmental processes that establish cell identity are thought to be robust to environmental perturbation, while those relating to body and organ growth show greater degrees of plasticity. However, examples of plastic patterning and robust organ growth demonstrate that this is not a hard-and-fast rule.In this review, we explore how the developmental context and the gene regulatory mechanisms underlying trait formation determine the impacts of the environment on development in insects. Furthermore, we outline future issues that need to be resolved to understand how the structure of signaling networks defines whether a trait displays plasticity or robustness.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-041620-083838
2021-01-07
2024-07-19
Loading full text...

Full text loading...

/deliver/fulltext/en/66/1/annurev-ento-041620-083838.html?itemId=/content/journals/10.1146/annurev-ento-041620-083838&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abouchar L, Petkova MD, Steinhardt CR, Gregor T 2014. Fly wing vein patterns have spatial reproducibility of a single cell. J. R. Soc. Interface 11:20140443
    [Google Scholar]
  2. 2. 
    Al-Saffar ZY, Grainger JNR, Aldrich J 1996. Temperature and humidity affecting development, survival and weight loss of the pupal stage of Drosophila melanogaster, and the influence of alternating temperature on the larvae. J. Therm. Biol. 21:389–96
    [Google Scholar]
  3. 3. 
    Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P 2002. Drosophila and the molecular genetics of pattern formation: genesis of the body plan. Molecular Biology of the Cell B Alberts, A Johnson, J Lewis, M Raff, K Roberts, P Walter, ch. NBK26906 New York: Garland Sci. , 4th ed..
    [Google Scholar]
  4. 4. 
    Alexandre C, Baena-Lopez A, Vincent JP 2014. Patterning and growth control by membrane-tethered Wingless. Nature 505:180–85
    [Google Scholar]
  5. 5. 
    Azevedo RBR, French V, Partridge L 1996. Thermal evolution of egg size in Drosophila melanogaster. Evolution 50:2338–45
    [Google Scholar]
  6. 6. 
    Beadle GW, Tatum EL, Clancy CW 1938. Food level in relation to rate of development and eye pigmentation in Drosophila melanogaster. Biol. Bull 75:447–62
    [Google Scholar]
  7. 7. 
    Booth DT, Kiddell K. 2007. Temperature and the energetics of development in the house cricket (Acheta domesticus). J. Insect Physiol. 53:950–53
    [Google Scholar]
  8. 8. 
    Bothma JP, Norstad MR, Alamos S, Garcia HG 2018. LlamaTags: a versatile tool to image transcription factor dynamics in live embryos. Cell 173:1810–22.e16
    [Google Scholar]
  9. 9. 
    Brakefield P, Kesbeke F, Koch P 1998. The regulation of phenotypic plasticity of eyespots in the butterfly Bicyclus anynana. Am. Nat 152:853–60
    [Google Scholar]
  10. 10. 
    Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R et al. 2001. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11:213–21
    [Google Scholar]
  11. 11. 
    Caldwell PE, Walkiewicz M, Stern M 2005. Ras activity in the Drosophila prothoracic gland regulates body size and developmental rate via ecdysone release. Curr. Biol. 15:1785–95
    [Google Scholar]
  12. 12. 
    Callier V, Shingleton AW, Brent CS, Ghosh SM, Kim J, Harrison JF 2013. The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila melanogaster. J. Exp. Biol 216:4334–40
    [Google Scholar]
  13. 13. 
    Campos-Ortega JA, Hartenstein V. 1985. The Embryonic Development of Drosophila melanogaster Berlin: Springer
    [Google Scholar]
  14. 14. 
    Carpenter SR. 1983. Resource limitation of larval treehole mosquitoes subsisting on beech detritus. Ecology 64:219–23
    [Google Scholar]
  15. 15. 
    Cheng LY, Bailey AP, Leevers SJ, Ragan TJ, Driscoll PC, Gould AP 2011. Anaplastic lymphoma kinase spare organ growth during nutrient restriction in Drosophila. Cell 146:435–47
    [Google Scholar]
  16. 16. 
    Cheung D, Ma J. 2015. Probing the impact of temperature on molecular events in a developmental system. Sci. Rep. 5:13124
    [Google Scholar]
  17. 17. 
    Cheung D, Miles C, Kreitman M, Ma J 2011. Scaling of the Bicoid morphogen gradient by a volume-dependent production rate. Development 138:2741–49
    [Google Scholar]
  18. 18. 
    Cheung D, Miles C, Kreitman M, Ma J 2014. Adaptation of the length scale and amplitude of the Bicoid gradient profile to achieve robust patterning in abnormally large Drosophila melanogaster embryos. Development 141:124–35
    [Google Scholar]
  19. 19. 
    Chong J, Amourda C, Saunders TE 2018. Temporal development of Drosophila embryos is highly robust across a wide temperature range. J. R. Soc. Interface 15:20180304
    [Google Scholar]
  20. 20. 
    Cohen SM. 1993. Imaginal disc development. The Development of Drosophila melanogaster 2 MA Bate 747–841 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
    [Google Scholar]
  21. 21. 
    Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C et al. 2005. Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310:667–70
    [Google Scholar]
  22. 22. 
    Connahs H, Tlili S, van Creij J, Loo TYJ, Banerjee TD et al. 2019. Activation of butterfly eyespots by Distal-less is consistent with a reaction-diffusion process. Development 146:dev169367
    [Google Scholar]
  23. 23. 
    Crick F. 1970. Diffusion in embryogenesis. Nature 225:420–42
    [Google Scholar]
  24. 24. 
    Cruz S, Romanoff A. 1944. Effect of oxygen concentration on the development of the chick embryo. Physiol. Zool. 17:184–87
    [Google Scholar]
  25. 25. 
    DeLalio LJ, Dion SM, Bootes AM, Smith WA 2015. Direct effects of hypoxia and nitric oxide on ecdysone secretion by insect prothoracic glands. J. Insect Physiol. 76:56–66
    [Google Scholar]
  26. 26. 
    Dubuis JO, Samanta R, Gregor T 2013. Accurate measurements of dynamics and reproducibility in small genetic networks. Mol. Syst. Biol. 9:639
    [Google Scholar]
  27. 27. 
    Durrieu L, Kirrmaier D, Schneidt T, Kats I, Raghavan S et al. 2018. Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis. Mol. Syst. Biol. 14:e8355
    [Google Scholar]
  28. 28. 
    Emlen DJ, Corley Lavine L, Ewen-Campen B 2007. On the origin and evolutionary diversification of beetle horns. PNAS 104:Suppl. 18661–68
    [Google Scholar]
  29. 29. 
    Félix MA, Wagner A. 2008. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity 100:132–40
    [Google Scholar]
  30. 30. 
    Forbes AJ, Lin H, Ingham PW, Spradling AC 1996. Hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122:1125–35
    [Google Scholar]
  31. 31. 
    Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitan-Espitia JD 2019. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. Lond. B 374:20180174
    [Google Scholar]
  32. 32. 
    Gancz D, Lengil T, Gilboa L 2011. Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLOS Biol 9:e1001202
    [Google Scholar]
  33. 33. 
    Garcia HG, Tikhonov M, Lin A, Gregor T 2013. Quantitative imaging of transcription in living Drosophila embryos links polymerase activity to patterning. Curr. Biol. 23:2140–45
    [Google Scholar]
  34. 34. 
    Géminard C, Rulifson EJ, Léopold P 2009. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10:199–207
    [Google Scholar]
  35. 35. 
    Ghosh SM, Testa ND, Shingleton AW 2013. Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster. Proc. R. Soc. B 280:20130174
    [Google Scholar]
  36. 36. 
    Gilbert SF. 2000. Developmental Biology Sunderland, MA: Sinauer Assoc.
    [Google Scholar]
  37. 37. 
    Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH 2002. Effects of size and temperature on developmental time. Nature 417:70–73
    [Google Scholar]
  38. 38. 
    Godt D, Laski FA. 1995. Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric à brac. Development 121:173–87
    [Google Scholar]
  39. 39. 
    Greene E. 1989. A diet-induced developmental polymorphism in a caterpillar. Science 243:643–46
    [Google Scholar]
  40. 40. 
    Gregor T, Bialek W, de Ruyter van Steveninck RR, Tank DW, Wieschaus EF 2005. Diffusion and scaling during early embryonic pattern formation. PNAS 102:18403–7
    [Google Scholar]
  41. 41. 
    Gregor T, McGregor AP, Wieschaus EF 2008. Shape and function of the Bicoid morphogen gradient in dipteran species with different sized embryos. Dev. Biol. 316:350–57
    [Google Scholar]
  42. 42. 
    Gregor T, Tank DW, Wieschaus EF, Bialek W 2007. Probing the limits to positional information. Cell 130:153–64
    [Google Scholar]
  43. 43. 
    Gregor T, Wieschaus EF, McGregor AP, Bialek W, Tank DW 2007. Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 130:141–52
    [Google Scholar]
  44. 44. 
    Grimm O, Coppey M, Wieschaus E 2010. Modelling the Bicoid gradient. Development 137:2253–64
    [Google Scholar]
  45. 45. 
    Hamaratoglu F, Affolter M, Pyrowolakis G 2014. Dpp/BMP signaling in flies: from molecules to biology. Semin. Cell Dev. Biol. 32:128–36
    [Google Scholar]
  46. 46. 
    Hariharan IK. 2015. Organ size control: lessons from Drosophila. Dev. Cell 34:255–65
    [Google Scholar]
  47. 47. 
    Helm BR, Rinehart JP, Yocum GD, Greenlee KJ, Bowsher JH 2017. Metamorphosis is induced by food absence rather than a critical weight in the solitary bee. Osmia lignaria. PNAS 114:10924–29
    [Google Scholar]
  48. 48. 
    Heming BS. 2003. Insect Development and Evolution Ithaca, NY: Cornell Univ. Press
    [Google Scholar]
  49. 49. 
    Hietakangas V, Cohen SM. 2009. Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43:386–410
    [Google Scholar]
  50. 50. 
    Hodin J, Riddiford LM. 2000. Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in drosophilids (Insecta: Diptera). Evolution 54:1638–53
    [Google Scholar]
  51. 51. 
    Houchmandzadeh B, Wieschaus E, Leibler S 2002. Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415:798–802
    [Google Scholar]
  52. 52. 
    Huang A, Amourda C, Zhang S, Tolwinski NS, Saunders TE 2017. Decoding temporal interpretation of the morphogen Bicoid in the early Drosophila embryo. eLife 6:e26258
    [Google Scholar]
  53. 53. 
    Huang A, Saunders TE. 2020. Embryonic geometry underlies phenotypic variation in decanalized conditions. eLife 9:e47380
    [Google Scholar]
  54. 54. 
    Huang A, Saunders TE. 2019. A matter of time: formation and interpretation of the Bicoid morphogen gradient. Curr. Top. Dev. Biol. 137:79–117
    [Google Scholar]
  55. 55. 
    Hudson A. 1966. Proteins in the haemolymph and other tissues of the developing tomato hornworm, Protoparce quinqumaculata Haworth. Can. J. Zool. 44:541–55
    [Google Scholar]
  56. 56. 
    Ikeya T, Galic M, Belawat P, Nairz K, Hafen E 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]
  57. 57. 
    Jaeger J. 2011. The gap gene network. Cell Mol. Life Sci. 68:243–74
    [Google Scholar]
  58. 58. 
    Jünger MA, Rintelen F, Stocker H, Wasserman JD, Végh M et al. 2003. The Drosophila Forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2:20
    [Google Scholar]
  59. 59. 
    Kerkis J. 1931. The growth of the gonads in Drosophila melanogaster. Genetics 16:212–24
    [Google Scholar]
  60. 60. 
    King RC. 1970. Ovarian Development in Drosophila melanogaster New York: Academic
    [Google Scholar]
  61. 61. 
    King RC, Aggarwal SK, Aggarwal U 1968. The development of the female Drosophila reproductive system. J. Morphol. 124:143–66
    [Google Scholar]
  62. 62. 
    Kooi RE, Brakefield PM. 1999. The critical period for wing pattern induction in the polyphenic tropical butterfly Bicyclus anynana (Satyrinae). J. Insect Physiol. 45:201–12
    [Google Scholar]
  63. 63. 
    Koyama T, Mendes CC, Mirth CK 2013. Mechanisms regulating nutrition-dependent developmental plasticity through organ-specific effects in insects. Front. Physiol. 4:263
    [Google Scholar]
  64. 64. 
    Koyama T, Mirth CK. 2018. Unravelling the diversity of mechanisms through which nutrition regulates body size in insects. Curr. Opin. Insect Sci. 25:1–8
    [Google Scholar]
  65. 65. 
    Koyama T, Rodrigues MA, Athanasiadis A, Shingleton AW, Mirth CK 2014. Nutritional control of body size through FoxO-Ultraspiracle mediated ecdysone biosynthesis. eLife 3:e03091
    [Google Scholar]
  66. 66. 
    Krieger JW, Singh AP, Bag N, Garbe CS, Saunders TE et al. 2015. Imaging fluorescence (cross-)correlation spectroscopy in live cells and organisms. Nat. Protoc. 10:1948–74
    [Google Scholar]
  67. 67. 
    Kulkarni A, Anderson AG, Merullo DP, Konopka G 2019. Beyond bulk: a review of single cell transcriptomics methodologies and applications. Curr. Opin. Biotechnol. 58:129–36
    [Google Scholar]
  68. 68. 
    Kuntz SG, Eisen MB. 2014. Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLOS Genet 10:e1004293
    [Google Scholar]
  69. 69. 
    Kuntz SG, Eisen MB. 2015. Oxygen changes drive non-uniform scaling in Drosophila melanogaster embryogenesis. F1000Res 4:1102
    [Google Scholar]
  70. 70. 
    Lander AD, Nie Q, Vargas B, Wan FY 2011. Size-normalized robustness of Dpp gradient in Drosophila wing imaginal disc. J. Mech. Mater. Struct. 6:321–50
    [Google Scholar]
  71. 71. 
    Li Q, Gong Z. 2015. Cold-sensing regulates Drosophila growth through insulin-producing cells. Nat. Commun. 6:10083
    [Google Scholar]
  72. 72. 
    Lucas T, Ferraro T, Roelens B, De Las Heras Chanes J, Walczak AM et al. 2013. Live imaging of bicoid-dependent transcription in Drosophila embryos. Curr. Biol. 23:2135–39
    [Google Scholar]
  73. 73. 
    Lucchetta EM, Carthew RW, Ismagilov RF 2009. The endo-siRNA pathway is essential for robust development of the Drosophila embryo. PLOS ONE 4:e7576
    [Google Scholar]
  74. 74. 
    Lucchetta EM, Lee JH, Fu LA, Patel NH, Ismagilov RF 2005. Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics. Nature 434:1134–38
    [Google Scholar]
  75. 75. 
    Lucchetta EM, Vincent ME, Ismagilov RF 2008. A precise Bicoid gradient is nonessential during cycles 11–13 for precise patterning in the Drosophila blastoderm. PLOS ONE 3:e3651
    [Google Scholar]
  76. 76. 
    Ludwig D, Cable R. 1933. The effect of alternating temperatures on the pupal development of Drosophila melanogaster Meigen. Physiol. Zool. 6:493–508
    [Google Scholar]
  77. 77. 
    Markow TA, Beall S, Matzkin LM 2009. Egg size, embryonic development time and ovoviviparity in Drosophila species. J. Evol. Biol. 22:430–34
    [Google Scholar]
  78. 78. 
    Mendes CC, Mirth CK. 2016. Stage-specific plasticity in ovary size is regulated by insulin/insulin-like growth factor and ecdysone signalling in Drosophila. Genetics 202:703–19
    [Google Scholar]
  79. 79. 
    Miner AL, Rosenberg AJ, Nijhout HF 2000. Control of growth and differentiation of the wing imaginal disk of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 46:251–58
    [Google Scholar]
  80. 80. 
    Mirth CK, Frankino WA, Shingleton AW 2016. Allometry and size control: What can studies of body size regulation teach us about the evolution of morphological scaling relationships?. Curr. Opin. Insect Sci. 13:93–98
    [Google Scholar]
  81. 81. 
    Mirth CK, Riddiford LM. 2007. Size assessment and growth control: how adult size is determined in insects. BioEssays 29:344–55
    [Google Scholar]
  82. 82. 
    Mirth CK, Shingleton AW. 2012. Integrating body and organ size in Drosophila: recent advances and outstanding problems. Front. Endocrinol. 3:49
    [Google Scholar]
  83. 83. 
    Mirth CK, Shingleton AW. 2019. Coordinating development: How do animals integrate plastic and robust developmental processes. Front. Cell Dev. Biol. 7:8
    [Google Scholar]
  84. 84. 
    Mirth CK, Truman JW, Riddiford LM 2005. The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr. Biol 15:1796–807
    [Google Scholar]
  85. 85. 
    Mirth CK, Truman JW, Riddiford LM 2009. The ecdysone receptor controls the post-critical weight switch to nutrition-independent differentiation in Drosophila wing imaginal discs. Development 136:2345–53
    [Google Scholar]
  86. 86. 
    Mlodzik M, Fjose A, Gehring WJ 1985. Isolation of caudal, a Drosophila homeo box-containing gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J 4:2961–69
    [Google Scholar]
  87. 87. 
    Monteiro A. 2017. Physiology and evolution of wing pattern plasticity in Bicyclus butterflies: a critical review of the literature. Diversity and Evolution of Butterfly Wing Patterns T Sekimura, HF Nijhout 91–105 Berlin: Springer
    [Google Scholar]
  88. 88. 
    Monteiro A, Tong X, Bear A, Liew SF, Bhardwaj S et al. 2015. Differential expression of ecdysone receptor leads to variation in phenotypic plasticity across serial homologs. PLOS Genet 11:e1005529
    [Google Scholar]
  89. 89. 
    Nijhout HF. 1979. Stretch-induced moulting in Oncopeltus fasciatus. J. Insect Physiol 25:277–81
    [Google Scholar]
  90. 90. 
    Nijhout HF. 1994. Insect Hormones Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  91. 91. 
    Nijhout HF. 1999. Control mechanisms of polyphenic development in insects. BioEssays 49:181–92
    [Google Scholar]
  92. 92. 
    Nijhout HF. 2003. The control of body size in insects. Dev. Biol. 261:1–9
    [Google Scholar]
  93. 93. 
    Nijhout HF, Callier V. 2013. A new mathematical approach for qualitative modeling of the insulin-TOR-MAPK network. Front. Physiol. 4:245
    [Google Scholar]
  94. 94. 
    Nijhout HF, Grunert LW. 2010. The cellular and physiological mechanism of wing-body scaling in Manduca sexta. Science 330:1693–95
    [Google Scholar]
  95. 95. 
    Nijhout HF, Sadre-Marandi F, Best J, Reed MC 2017. Systems biology of phenotypic robustness and plasticity. Integr. Comp. Biol. 57:171–84
    [Google Scholar]
  96. 96. 
    Nijhout HF, Williams CM. 1974. Control of molting 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]
  97. 97. 
    Nijhout HF, Williams CM. 1974. Control of molting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J. Exp. Biol. 61:481–91
    [Google Scholar]
  98. 98. 
    Noor MA, Parnell RS, Grant BS 2008. A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars. PLOS ONE 3:e3142
    [Google Scholar]
  99. 99. 
    Ogden SK, Ascano M Jr., Stegman MA, Robbins DJ 2004. Regulation of Hedgehog signaling: a complex story. Biochem. Pharmacol 67:805–14
    [Google Scholar]
  100. 100. 
    Oldham S, Hafen E. 2003. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol 13:79–85
    [Google Scholar]
  101. 101. 
    Oliveira MM, Shingleton AW, Mirth CK 2014. Coordination of wing and whole-body development at developmental milestones ensures robustness against environmental and physiological pertubations. PLOS Genet 10:e1004408
    [Google Scholar]
  102. 102. 
    Oostra V, de Jong MA, Invergo BM, Kesbeke F, Wende F et al. 2011. Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Proc. Biol. Sci. 278:789–97
    [Google Scholar]
  103. 103. 
    Petkova MD, Little SC, Liu F, Gregor T 2014. Maternal origins of developmental reproducibility. Curr. Biol. 24:1283–88
    [Google Scholar]
  104. 104. 
    Petkova MD, Tkacik G, Bialek W, Wieschaus EF, Gregor T 2019. Optimal decoding of cellular identities in a genetic network. Cell 176:844–55.e15
    [Google Scholar]
  105. 105. 
    Posadas DM, Carthew RW. 2014. MicroRNAs and their roles in developmental canalization. Curr. Opin. Genet. Dev. 27:1–6
    [Google Scholar]
  106. 106. 
    Powsner L. 1935. The effects of temperature on the durations of the developmental stages of Drosophila melanogaster. Physiol. Zool 8:474–520
    [Google Scholar]
  107. 107. 
    Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC et al. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–6
    [Google Scholar]
  108. 108. 
    Richmond RC, Gerking JL. 1979. Oviposition site preference in Drosophila. Behav. Genet 9:233–41
    [Google Scholar]
  109. 109. 
    Rogers KW, Schier AF. 2011. Morphogen gradients: from generation to interpretation. Annu. Rev. Cell Dev. Biol. 27:377–407
    [Google Scholar]
  110. 110. 
    Rolff J, Johnston PR, Reynolds S 2019. Complete metamorphosis of insects. Philos. Trans. R. Soc. Lond. B 374:20190063
    [Google Scholar]
  111. 111. 
    Sahut-Barnola I, Godt D, Laski FA, Couderc JL 1995. Drosophila ovary morphogenesis: analysis of terminal filament formation and identification of a gene required for this process. Dev. Biol. 170:127–35
    [Google Scholar]
  112. 112. 
    Sarikaya DP, Belay AA, Ahuja A, Dorta A, Li DAG, Extavour CG 2012. The roles of cell size and cell number in determining ovariole number in Drosophila. Dev. Biol 363:279–89
    [Google Scholar]
  113. 113. 
    Sato T, Suzuki A. 2001. Effect of starvation and feeding of larvae during 4th stadia on pupation and adult size in Dacne picta (Coleoptera: Erotylidae). Appl. Entomol. Zool. 36:189–97
    [Google Scholar]
  114. 114. 
    Seger R, Krebs EG. 1995. The MAPK signaling cascade. FASEB J 9:726–35
    [Google Scholar]
  115. 115. 
    Setiawan L, Pan X, Woods AL, O'Connor MB, Hariharan IK 2018. The BMP2/4 ortholog Dpp can function as an inter-organ signal that regulates developmental timing. Life Sci. Alliance 1:e201800216
    [Google Scholar]
  116. 116. 
    Shafiei M, Moczek AP, Nijhout HF 2001. Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiol. Entomol. 26:173–80
    [Google Scholar]
  117. 117. 
    Shingleton AW, Das J, Vinicius L, Stern DL 2005. The temporal requirements for insulin signalling during development in Drosophila. PLOS Biol 3:e289
    [Google Scholar]
  118. 118. 
    Simon MC, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat. Rev. Mol. Cell Biol. 9:285–96
    [Google Scholar]
  119. 119. 
    Snell-Rood EC, Moczek AP. 2012. Insulin signaling as a mechanism underlying developmental plasticity: the role of FOXO in a nutritional polyphenism. PLOS ONE 7:e34857
    [Google Scholar]
  120. 120. 
    Stieper BC, Kupershtok M, Driscoll MV, Shingleton AW 2008. Imaginal discs regulate developmental timing in Drosophila melanogaster. Dev. Biol 321:18–26
    [Google Scholar]
  121. 121. 
    Swarup S, Verheyen EM. 2012. Wnt/Wingless signaling in Drosophila. Cold Spring Harb. Perspect. Biol 4:a007930
    [Google Scholar]
  122. 122. 
    Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shingleton AW 2011. FOXO regulates organ-specific phenotypic plasticity in Drosophila. PLOS Genet 7:e1002373
    [Google Scholar]
  123. 123. 
    Texada MJ, Jorgensen AF, Christensen CF, Koyama T, Malita A et al. 2019. A fat-tissue sensor couples growth to oxygen availability by remotely controlling insulin secretion. Nat. Commun. 10:1955
    [Google Scholar]
  124. 124. 
    Truman JW, Riddiford LM. 2019. The evolution of insect metamorphosis: a developmental and endocrine view. Philos. Trans. R. Soc. Lond. B 374:20190070
    [Google Scholar]
  125. 125. 
    Umulis DM, Othmer HG. 2013. Mechanisms of scaling in pattern formation. Development 140:4830–43
    [Google Scholar]
  126. 126. 
    Wartlick O, Mumcu P, Kicheva A, Bittig T, Seum C et al. 2011. Dynamics of Dpp signaling and proliferation control. Science 331:1154–59
    [Google Scholar]
  127. 127. 
    Wigglesworth VB. 1934. Physiology of ecdysis in Rhodnius prolixus (Hemiptera)—II. Factors controlling moulting and metamorphosis. Q. J. Microsc. Sci. 77:191–222
    [Google Scholar]
  128. 128. 
    Wimberger PH. 1992. Plasticity of fish body shape: the effects of diet, development, family and age in two species of Geophagus (Pisces: Cichlidae). Biol. J. Linn. Soc. 45:197–218
    [Google Scholar]
  129. 129. 
    Zoller B, Little SC, Gregor T 2018. Diverse spatial expression patterns emerge from unified kinetics of transcriptional bursting. Cell 175:835–47.e25
    [Google Scholar]
  130. 130. 
    Zuo W, Moses ME, West GB, Hou C, Brown JH 2012. A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc. Biol. Sci. 279:1840–46
    [Google Scholar]
/content/journals/10.1146/annurev-ento-041620-083838
Loading
/content/journals/10.1146/annurev-ento-041620-083838
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