Asymmetric flies: The control of developmental noise in Drosophila

Fly

Volumn 7, Issue 2, 2013, Pages

  Debat, Vincent ^a   Peronnet, Frédérique ^b  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Canalization; Cyclin G; Developmental stability; Drosophila; Fluctuating asymmetry; Geometric morphometrics; Robustness; Shape; Size; Wing

Indexed keywords

CYCLIN G; DROSOPHILA PROTEIN;

ANATOMY AND HISTOLOGY; ANIMAL; ASYMMETRIC CELL DIVISION; DROSOPHILA; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGAN SIZE; PHENOTYPE; PHYSIOLOGY; STATISTICS; ARTICLE; CANALIZATION; DEVELOPMENTAL STABILITY; FLUCTUATING ASYMMETRY; FORELIMB; GEOMETRIC MORPHOMETRICS; HISTOLOGY; ROBUSTNESS; SHAPE; SIZE;

ANIMALS; ASYMMETRIC CELL DIVISION; CYCLIN G; DROSOPHILA; DROSOPHILA PROTEINS; ORGAN SIZE; PHENOTYPE; STOCHASTIC PROCESSES;

CANALIZATION; CYCLIN G; DEVELOPMENTAL STABILITY; DROSOPHILA; FLUCTUATING ASYMMETRY; GEOMETRIC MORPHOMETRICS; ROBUSTNESS; SHAPE; SIZE; WING;

EID: 84892861817     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: None     Document Type: Article

References (84)

1. Debat V, Bloyer S, Faradji F, Gidaszewski N, Navarro N, Orozco-Terwengel P, et al. Developmental stability: a major role for Cyclin G in Drosophila melanogaster. PLoS Genet 2011; 7:e1002314; PMID:21998598; http://dx.doi.org/10.1371/journal.pgen.1002314.
2. Waddington CH. Canalization of development and the inheritance of acquired characters. Nature 1942; 150:563-653; http://dx.doi.org/10.1038/150563a0.
3. Flatt T. The evolutionary genetics of canalization. Q Rev Biol 2005; 80:287-316; PMID:16250465; http://dx.doi.org/10.1086/432265.
4. Nijhout F, Davidowitz G. Developmental perspectives on phenotypic variation, canalization, and fluctuating asymmetry. In: Polak M, ed. Developmental instability, causes and consequences. Oxford, UK: Oxford University Press, 2003:3-13.
5. Debat V, David P. Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 2001; 16:555-61; http://dx.doi.org/10.1016/S0169-5347(01)02266-2.
6. Dworkin I. Canalization, cryptic variation and developmental buffering: a critical examination and analytical perspective. In: Hallgrimsson B, Hall BK, eds. Variation: a central concept in biology. London UK: Elsevier Academic Press, 2005:131-55.
7. Waddington CH. The strategy of the genes: a discussion of some aspects of theoretical biology. New York, NY: MacMillan, 1957.
8. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998; 396:336-42; PMID:9845070; http://dx.doi.org/10.1038/24550.
9. Gilbert SF. Diachronic biology meets evo-devo: CH Waddington's approach to evolutionary developmental biology. Am Zool 2000; 40:729-37; http://dx.doi.org/10.1668/0003-1569(2000)040[0729:DBMEDC]2.0.CO;2.
10. Gibson G, Dworkin I. Uncovering cryptic genetic variation. Nat Rev Genet 2004; 5:681-90; PMID:15372091; http://dx.doi.org/10.1038/nrg1426.
11. McGuigan K, Sgrò CM. Evolutionary consequences of cryptic genetic variation. Trends Ecol Evol 2009; 24:305-11; PMID:19328588; http://dx.doi.org/10.1016/j.tree.2009.02.001.
12. Roff DA. Evolutionary quantitative genetics. New York, NY: Chapman and Hall, 1997.
13. Palmer AR, Strobeck C. Fluctuating asymmetry-Measurement, Analysis, Patterns. Annual Review of Ecol. Syst 1986; 17:391-421.
14. McAdams HH, Arkin A. It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet 1999; 15:65-9; PMID:10098409; http://dx.doi.org/10.1016/S0168-9525(98)01659-X.
15. Scharloo W. Canalization: genetic and developmental aspects. Annu Rev Ecol Syst 1991; 22:65-93; http://dx.doi.org/10.1146/annurev.es.22.110191.000433.
16. Alibert P, Auffray J. Genomic coadaptation, outbreeding depression and developmental instability. In: Polak M, ed. Developmental instability: causes and consequences. Oxford, UK: Oxford University Press, 2003:116-134.
17. Lewontin RC. The triple helix: gene, organism, and environment. Cambridge, MA: Harvard University Press, 2000.
18. Kupiec JJ. A Darwinian theory for the origin of cellular differentiation. Mol Gen Genet 1997; 255:201-8; PMID:9236778; http://dx.doi.org/10.1007/s004380050490.
19. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 2005; 6:451-64; PMID:15883588; http://dx.doi.org/10.1038/nrg1615.
20. Wernet MF, Mazzoni EO, Celik A, Duncan DM, Duncan I, Desplan C. Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 2006; 440:174-80; PMID:16525464; http://dx.doi.org/10.1038/nature04615.
21. Johnston RJ Jr., Desplan C. Preview. A penetrating look at stochasticity in development. Cell 2010; 140:610-2; PMID:20211129; http://dx.doi.org/10.1016/j.cell.2010.02.018.
22. Rutherford SL. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 2003; 4:263-74; PMID:12671657; http://dx.doi.org/10.1038/nrg1041.
23. Dickinson WJ, Seger J. Cause and effect in evolution. Nature 1999; 399:30; PMID:10331386; http://dx.doi.org/10.1038/19894.
24. Fares MA, Ruiz-González MX, Moya A, Elena SF, Barrio E. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 2002; 417:398; PMID:12024205; http://dx.doi.org/10.1038/417398a.
25. Hornstein E, Shomron N. Canalization of development by microRNAs. Nat Genet 2006; 38(Suppl):S20-4; PMID:16736020; http://dx.doi.org/10.1038/ng1803.
26. True HL, Lindquist SL. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000; 407:477-83; PMID:11028992; http://dx.doi.org/10.1038/35035005.
27. Masel J. Cryptic genetic variation is enriched for potential adaptations. Genetics 2006; 172:1985-91; PMID:16387877; http://dx.doi.org/10.1534/genetics.105.051649.
28. Modrek B, Lee CJ. Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 2003; 34:177-80; PMID:12730695; http://dx.doi.org/10.1038/ng1159.
29. Siegal ML, Bergman A. Waddington's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci U S A 2002; 99:10528-32; PMID:12082173; http://dx.doi.org/10.1073/pnas.102303999.
30. Wagner A. Robustness and evolvability: a paradox resolved. Proc Biol Sci 2008; 275:91-100; PMID:17971325; http://dx.doi.org/10.1098/rspb.2007.1137.
31. von Dassow G, Meir E, Munro EM, Odell GM. The segment polarity network is a robust developmental module. Nature 2000; 406:188-92; PMID:10910359; http://dx.doi.org/10.1038/35018085.
32. Kerszberg M. Noise, delays, robustness, canalization and all that. Curr Opin Genet Dev 2004; 14:440-5; PMID:15261662; http://dx.doi.org/10.1016/j.gde.2004.06.001.
33. Hermisson J, Wagner GP. The population genetic theory of hidden variation and genetic robustness. Genetics 2004; 168:2271-84; PMID:15611191; http://dx.doi.org/10.1534/genetics.104.029173.
34. Rutherford S, Knapp JR, Csermely P. Hsp90 and developmental networks. Adv Exp Med Biol 2007; 594:190-7; PMID:17205685; http://dx.doi.org/10.1007/978-0-387-39975-1_16.
35. Jeong H, Mason SP, Barabási AL, Oltvai ZN. Lethality and centrality in protein networks. Nature 2001; 411:41-2; PMID:11333967; http://dx.doi.org/10.1038/35075138.
36. Levy SF, Siegal ML. Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 2008; 6:e264; PMID:18986213; http://dx.doi.org/10.1371/journal.pbio.0060264.
37. Meiklejohn CD, Hartl DL. A single mode of canalization. Trends Ecol Evol 2002; 17:468-73; http://dx.doi.org/10.1016/S0169-5347(02)02596-X.
38. Masel J, Siegal ML. Robustness: mechanisms and consequences. Trends Genet 2009; 25:395-403; PMID:19717203; http://dx.doi.org/10.1016/j.tig.2009.07.005.
39. Cooper TF, Morby AP, Gunn A, Schneider D. Effect of random and hub gene disruptions on environmental and mutational robustness in Escherichia coli. BMC Genomics 2006; 7:237; PMID:16982007; http://dx.doi.org/10.1186/1471-2164-7-237.
40. Van Valen L. A study of fluctuating asymmetry. Evolution 1962; 16:125-42; http://dx.doi.org/10.2307/2406192.
41. Palmer AR. Fluctuating asymmetry analysis: a primer. In: Markow T, ed. Developmental instability: its origins and evolutionary implications. Dordrecht, Netherlands: Kluwer Academic Publishers, 1994:335-64.
42. Willmore KE, Hallgrimsson B. Within individual variation: developmental noise versus developmental stability. In: Hallgrimsson B, Hall BK, eds. Variation: a central concept in biology. London UK: Elsevier Academic Press, 2005:191-215.
43. Møller AP, Swaddle JP. Asymmetry, developmental stability and evolution. Oxford, UK: Oxford University Press, 1997.
44. Houle D. High enthusiasm and low R-squared. Asymmetry, developmental stability, and evolution, by A.P. Møller and J. P. Swaddle. Evolution 1998; 52:1872-6; http://dx.doi.org/10.2307/2411361.
45. Leamy LJ, Routman EJ, Cheverud JM. An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution 2002; 56:642-53; PMID:11989692.
46. Leamy LJL, Klingenberg CPK. The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol Syst 2005; 36:1-21; http://dx.doi.org/10.1146/annurev.ecolsys.36.102003.152640.
47. Burgio G, Baylac M, Heyer E, Montagutelli X. Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between C57BL/6 and mice of the mus spretus species. Evolution 2009; 63:2668-86; PMID:19490077; http://dx.doi.org/10.1111/j.1558-5646.2009.00737.x.
48. Gomez FH, Norry FM. Is the number of possible QTL for asymmetry phenotypes dependent on thermal stress? J Therm Biol 2012; 37:1-5; http://dx.doi.org/10.1016/j.jtherbio.2011.10.001.
49. Whitlock M. The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc Biol Sci 1996; 263:849-53; PMID:8786993; http://dx.doi.org/10.1098/rspb.1996.0125.
50. Van Dongen S. How repeatable is the estimation of developmental stability by fluctuating asymmetry? Proc Biol Sci 1998; 265:1423-7; http://dx.doi.org/10.1098/rspb.1998.0452.
51. Fuller RC, Houle D. Inheritance of developmental instability. In: Polak M, ed. Developmental instability: causes and consequences. Oxford, UK: Oxford University Press, 2003:157-183.
52. Breuker CJ, Patterson JS, Klingenberg CP. A single basis for developmental buffering of Drosophila wing shape. PLoS One 2006; 1:e7; PMID:17183701; http://dx.doi.org/10.1371/journal.pone.0000007.
53. Takahashi KH, Okada Y, Teramura K. Genome-wide deficiency mapping of the regions responsible for temporal canalization of the developmental processes of Drosophila melanogaster. J Hered 2011; 102:448-57; PMID:21525178; http://dx.doi.org/10.1093/jhered/esr026.
54. Vangestel C, Mergeay J, Dawson DA, Vandomme V, Lens L. Developmental stability covaries with genome-wide and single-locus heterozygosity in house sparrows. PLoS One 2011; 6:e21569; PMID:21747940; http://dx.doi.org/10.1371/journal.pone.0021569.
55. Wolpert L. Arms and the man: the problem of symmetric growth. PLoS Biol 2010; 8:e1000477; PMID:20838659; http://dx.doi.org/10.1371/journal.pbio.1000477.
56. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci U S A 2003; 100:13396-401; PMID:14595030; http://dx.doi.org/10.1073/pnas.1835613100.
57. Debat V, Milton CC, Rutherford S, Klingenberg CP, Hoffmann AA. Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution 2006; 60:2529-38; PMID:17263114.
58. Takahashi KH, Rako L, Takano-Shimizu T, Hoffmann AA, Lee SF. Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol Biol 2010; 10:284; PMID:20846409; http://dx.doi.org/10.1186/1471-2148-10-284.
59. Takahashi KH, Daborn PJ, Hoffmann AA, Takano-Shimizu T. Environmental stress-dependent effects of deletions encompassing Hsp70Ba on canalization and quantitative trait asymmetry in Drosophila melanogaster. PLoS One 2011; 6:e17295; PMID:21541022; http://dx.doi.org/10.1371/journal.pone.0017295.
60. Batterham P, Davies AG, Game AY, McKenzie JA. Asymmetry--where evolutionary and developmental genetics meet. Bioessays 1996; 18:841-5; PMID:8885722; http://dx.doi.org/10.1002/bies.950181011.
61. Salvaing J, Nagel AC, Mouchel-Vielh E, Bloyer S, Maier D, Preiss A, et al. The enhancer of trithorax and polycomb corto interacts with cyclin G in Drosophila. PLoS One 2008; 3:e1658; PMID:18286205; http://dx.doi.org/10.1371/journal.pone.0001658.
62. Salvaing J, Mouchel-Vielh E, Bloyer S, Preiss A, Peronnet F. Regulation of Abd-B expression by Cyclin G and Corto in the abdominal epithelium of Drosophila. Hereditas 2008; 145:138-46; PMID:18667003; http://dx.doi.org/10.1111/j.0018-0661.2008.02067.x.
63. Faradji F, Bloyer S, Dardalhon-Cuménal D, Randsholt NB, Peronnet F. Drosophila melanogaster Cyclin G coordinates cell growth and cell proliferation. Cell Cycle 2011; 10:805-18; PMID:21311225; http://dx.doi.org/10.4161/cc.10.5.14959.
64. Klingenberg CP. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 2010; 11:623-35; PMID:20697423.
65. Simpson P, Woehl R, Usui K. The development and evolution of bristle patterns in Diptera. Development 1999; 126:1349-64; PMID:10068629.
66. Milton CC, Ulane CM, Rutherford S. Control of canalization and evolvability by Hsp90. PLoS One 2006; 1:e75; PMID:17183707; http://dx.doi.org/10.1371/journal.pone.0000075.
67. Clarke GM. The genetic basis of developmental stability. V. Inter-and intra-individual character variation. Heredity 1998; 80:562-7; http://dx.doi.org/10.1046/j.1365-2540.1998.00294.x.
68. Breno M, Leirs H, Van Dongen S. No relationship between canalization and developmental stability of the skull in a natural population of Mastomys natalensis (Rodentia: Muridae). Biol J Linn Soc Lond 2011; 104:207-16; http://dx.doi.org/10.1111/j.1095-8312.2011.01702.x.
69. Parker J. Morphogens, nutrients, and the basis of organ scaling. Evol Dev 2011; 13:304-14; PMID:21535468; http://dx.doi.org/10.1111/j.1525-142X.2011.00481.x.
70. García-Bellido A. The cellular and genetic bases of organ size and shape in Drosophila. Int J Dev Biol 2009; 53:1291-303; PMID:19924628; http://dx.doi.org/10.1387/ijdb.072459ag.
71. Parker NF, Shingleton AW. The coordination of growth among Drosophila organs in response to localized growth-perturbation. Dev Biol 2011; 357:318-25; PMID:21777576; http://dx.doi.org/10.1016/j.ydbio.2011.07.002.
72. Garelli A, Gontijo AM, Miguela V, Caparros E, Dominguez M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 2012; 336:579-82; PMID:22556250; http://dx.doi.org/10.1126/science.1216735.
73. Colombani J, Andersen DS, Léopold P. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 2012; 336:582-5; PMID:22556251; http://dx.doi.org/10.1126/science.1216689.
74. Morata G, Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Dev Biol 1975; 42:211-21; PMID:1116643; http://dx.doi.org/10.1016/0012-1606(75)90330-9.
75. de Beco S, Ziosi M, Johnston LA. New frontiers in cell competition. Dev Dyn 2012; 241:831-41; PMID:22438309; http://dx.doi.org/10.1002/dvdy.23783.
76. Neto-Silva RM, Wells BS, Johnston LA. Mechanisms of growth and homeostasis in the Drosophila wing. Annu Rev Cell Dev Biol 2009; 25:197-220; PMID:19575645; http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175242.
77. de la Cova C, Abril M, Bellosta P, Gallant P, Johnston LA. Drosophila myc regulates organ size by inducing cell competition. Cell 2004; 117:107-16; PMID:15066286; http://dx.doi.org/10.1016/S0092-8674(04)00214-4.
78. Milán M, Campuzano S, García-Bellido A. Developmental parameters of cell death in the wing disc of Drosophila. Proc Natl Acad Sci U S A 1997; 94:5691-6; PMID:9159134; http://dx.doi.org/10.1073/pnas.94.11.5691.
79. Martín FA, Peréz-Garijo A, Morata G. Apoptosis in Drosophila: compensatory proliferation and undead cells. Int J Dev Biol 2009; 53:1341-7; PMID:19247932; http://dx.doi.org/10.1387/ijdb.072447fm.
80. Bondar T, Medzhitov R. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 2010; 6:309-22; PMID:20362536; http://dx.doi.org/10.1016/j.stem.2010.03.002.
81. Mesquita D, Dekanty A, Milán M. A dp53-dependent mechanism involved in coordinating tissue growth in Drosophila. PLoS Biol 2010; 8:e1000566; PMID:21179433; http://dx.doi.org/10.1371/journal.pbio.1000566.
82. Coléno-Costes A, Jang SM, de Vanssay A, Rougeot J, Bouceba T, Randsholt NB, et al. New partners in regulation of gene expression: the enhancer of Trithorax and Polycomb Corto interacts with methylated ribosomal protein l12 via its chromodomain. PLoS Genet 2012; 8:e1003006; PMID:23071455; http://dx.doi.org/10.1371/journal.pgen.1003006.
83. Miller-Jensen K, Dey SS, Schaffer DV, Arkin AP. Varying virulence: epigenetic control of expression noise and disease processes. Trends Biotechnol 2011; 29:517-25; PMID:21700350; http://dx.doi.org/10.1016/j.tibtech.2011.05.004.
84. Shingleton AW, Tang HY. Plastic flies: The regulation and evolution of trait variability in Drosophila. Fly (Austin) 2012; 6:1-6; PMID:22705976.