Robustness and evolution: Concepts, insights and challenges from a developmental model system

Heredity

Volumn 100, Issue 2, 2008, Pages 132-140

  Felix M A ^a   Wagner, A ^b  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

C. elegans; Cryptic variation; Environment evolution; Robustness; Vulva

Indexed keywords

ADAPTATION; EVOLUTION; NATURAL SELECTION; NEMATODE; PERSISTENCE; PERTURBATION;

ANIMAL; CAENORHABDITIS ELEGANS; EVOLUTION; FEMALE; GENETICS; PRENATAL DEVELOPMENT; SHORT SURVEY; VULVA;

ANIMALS; CAENORHABDITIS ELEGANS; EVOLUTION; FEMALE; VULVA;

CAENORHABDITIS ELEGANS;

EID: 38549096995     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/sj.hdy.6800915     Document Type: Short Survey

References (79)

1. Ancel Meyers L, Bull JJ (2002). Fighting change with change: adaptive variation in an uncertain world. TREE 17: 551-557.
2. Azevedo RB, Lohaus R, Srinivasan S, Dang KK, Burch CL (2006). Sexual reproduction selects for robustness and negative epistasis in artificial gene networks. Nature 440: 87-90.
3. Bagheri-Chaichian H, Hermisson J, Vaisnys JR, Wagner GP (2003). Effects of epistasis on phenotypic robustness in metabolic pathways. Math Biosci 184: 27-51.
4. Barkai N, Leibler S (1997). Robustness in simple biochemical networks. Nature 387: 913-917.
5. Berset T, Hoier EF, Battu G, Canevascini S, Hajnal A (2001). Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291: 1055-1058.
6. Berset TA, Hoier EF, Hajnal A (2005). The C. elegans homolog of the mammalian tumor suppressor Dep-1/Scc1 inhibits EGFR signaling to regulate binary cell fate decisions. Genes Dev 19: 1328-1340.
7. Chen N, Greenwald I (2004). The lateral signal for LIN-12/Notch in C. elegans vulval development comprises redundant secreted and transmembrane DSL proteins. Dev Cell 6: 183-192.
8. de Visser JA, Hermisson J, Wagner GP, Ancel Meyers L, Bagheri-Chaichian H, Blanchard JL et al. (2003). Perspective: evolution and detection of genetic robustness. Evolution 57: 1959-1972.
9. Debat V, David P (2001). Mapping phenotypes: canalization, plasticity and developmental stability. TREE 16: 555-561.
10. Delattre M, Félix M-A (2001). Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr Biol 11: 631-643.
11. Denver DR, Morris K, Lynch M, Thomas WK (2004). High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430: 679-682.
12. Dworkin I (2005a). Canalization, cryptic variation, and developmental buffering: a critical examination and analytical perspective. In: Hallgrimsson B, Hall BK (eds). Variation - A Central Concept in Biology. Elsevier Inc.: Amsterdam. pp 131-158.
13. Dworkin I (2005b). A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster. Evolution 59: 1500-1509.
14. Dworkin I, Palsson A, Birdsall K, Gibson G (2003). Evidence that Egfr contributes to cryptic genetic variation for photoreceptor determination in natural populations of Drosophila melanogaster. Curr Biol 13: 1888-1893.
15. Eisenmann DM, Maloof JN, Simske JS, Kenyon C, Kim SK (1998). The β-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development 125: 3667-3680.
16. Eldar A, Dorfman R, Weiss D, Ashe H, Shilo BZ, Barkai N (2002). Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 419: 304-308.
17. Eldar A, Rosin D, Shilo B-Z, Barkai N (2003). Self-enhanced ligand degradation underlies robustness of morphogen gradients. Dev Cell 5: 635-646.
18. Félix M-A (1999). Evolution of developmental mechanisms in nematodes. J Exp Zool (Mol Dev Evol) 28: 3-18.
19. Félix M-A, Sternberg PW (1997). Two nested gonadal inductions of the vulva in nematodes. Development 124: 253-259.
20. Ferguson E, Horvitz HR (1985). Identification and characterization of 22 genes that affect the vulval cell lineages of Caenorhabditis elegans. Genetics 110: 17-72.
21. Ferguson EL, Horvitz HR (1989). The Multivulva phenotype of certain C. elegans mutants results from defects in two functionally-redundant pathways. Genetics 123: 109-121.
22. Flatt T (2005). The evolutionary genetics of canalization. Q Rev Biol 80: 287-316.
23. Gavrilets S (2004). Fitness Landscapes and the Origin of Species. University Presses of California: Columbia and Princeton. p 432.
24. Gerhart J, Kirschner M (1997). Cells, Embryos and Evolution. Blackwell Science, Inc.: Oxford. p 641.
25. Gibson G, Dworkin I (2004). Uncovering cryptic genetic variation. Nat Rev Genet 5: 681-690.
26. Gibson G, Hogness DS (1996). Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Nature 271: 200-203.
27. Gibson G, Wagner G (2000). Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22: 372-380.
28. Giurumescu CA, Sternberg PW, Asthagiri AR (2006). Intercellular coupling amplifies fate segregation during Caenorhabditis elegans vulval development. Proc Natl Acad Sci USA 103: 1331-1336.
29. Hajnal A, Whitfield CW, Kim SK (1997). Inhibition of Caenorhabditis elegans vulval induction by gap-1 and by let-23 receptor tyrosine kinase. Genes Dev 11: 2715-2728.
30. Hartl DL, Clark AG (1997). Principles of Population Genetics. Sinauer Associates, Inc.: Sunderland, MA. p 542.
31. Hartl DL, Dykhuizen DE, Dean AM (1985). Limits of adaptation: the evolution of selective neutrality. Genetics 111: 655-674.
32. Hopper NA, Lee J, Sternberg PW (2000). ARK-1 inhibits EGFR signaling in C. elegans. Mol Cell 6: 65-75.
33. Houle D (1992). Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
34. Houle D (1998). How should we explain variation in the genetic variance of traits? Genetica 102-103: 241-253.
35. Kacser H, Burns JA (1981). The molecular basis of dominance. Genetics 97: 639-666.
36. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
37. Kao G, Tuck S, Baillie D, Sundaram MV (2004). C. elegans SUR-6/PR55 cooperates with LET-92/protein phosphatase 2A and promotes Raf activity independently of inhibitory Akt phosphorylation sites. Development 131: 755-765.
38. Katz WS, Hill RJ, Clandinin TR, Sternberg PW (1995). Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell 82: 297-307.
39. Kenyon C (1995). A perfect vulva every time: gradients and signalling cascades in C. elegans. Cell 82: 171-174.
40. Koga M, Ohshima Y (1995). Mosaic analysis of the let-23 gene function in vulval induction of Caenorhabditis elegans. Development 121: 2655-2666.
41. Krakauer DC, Nowak MA (1999). Evolutionary preservation of redundant duplicated genes. Sem Cell Dev Biol 10: 555-559.
42. Krakauer DC, Plotkin JB (2002). Redundancy, antiredundancy, and the robustness of genomes. Proc Natl Acad Sci USA 99: 1405-1409.
43. Lynch M, Blanchard JL, Houle D, Kibota T, Schultz S, Vassileva L et al. (1999). Spontaneous deleterious mutation. Evolution 53: 645-663.
44. McAdams HH, Arkin A (1999). It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet 15: 65-69.
45. Meiklejohn CD, Hartl DL (2002). A single mode of canalization. TREE 17: 468-473.
46. Meir E, von Dassow G, Munro E, Odell GM (2002). Robustness, flexibility, and the role of lateral inhibition in the neurogenic network. Curr Biol 12: 778-786.
47. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA (2003). Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci USA 100: 13396-13401.
48. Moghal N, Garcia LR, Khan LA, Iwasaki K, Sternberg PW (2003). Modulation of EGF receptor-mediated vulva development by the heterotrimeric G-protein Gaq and excitable cells in C. elegans. Development 130: 4553-4566.
49. Nijhout HF, Berg AM (2003). A mechanistic study of evolvability using the mitogen-activated protein kinase cascade. Evol Dev 5: 281-294.
50. Ohmachi M, Rocheleau C, Church D, Lambie E, Schedl T, Sundaram M (2002). C. elegans ksr-1 and ksr-2 have both unique and redundant functions and are required for MPK-1 ERK phosphorylation. Curr Biol 12: 427-433.
51. Pigliucci M(2005). Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20: 481-486.
52. Polaczyk PJ, Gasperini R, Gibson G (1998). Naturally occurring genetic variation affects Drosophila photoreceptor determination. Dev Genes Evol 207: 462-470.
53. Proulx SR, Phillips PC (2005). The opportunity for canalization and the evolution of genetic networks. Am Naturalist 165: 147-162.
54. Riddle DL, Albert PS (1997). Genetic and environmental regulation of dauer larva development. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds). C. elegans II. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY. pp 739-768.
55. Rutherford SL (2000). From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays 22: 1095-1105.
56. Shaye DD, Greenwald I (2002). Endocytosis-mediated down-regulation of LIN-12/Notch upon Ras activation in Caenorhabditis elegans. Nature 420: 686-690.
57. Siegal ML, Bergman A (2002). Waddington's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci USA 99: 10528-10532.
58. Simske JS, Kim SK (1995). Sequential signalling during Caenorhabditis elegans vulval induction. Nature 375: 142-146.
59. Sommer RJ (2000). Evolution of nematode development. Curr Opin Gen Dev 10: 443-448.
60. Sommer RJ, Sternberg PW (1994). Changes of induction and competence during the evolution of vulva development in nematodes. Science 265: 114-118.
61. Sternberg PW (2005). Vulval development. In: WormBook (ed). The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.6.1, http://www.wormbook.org.
62. Stigler SM (1995). Galton and identification by fingerprints. Genetics 140: 857-860.
63. Sulston J, Horvitz HR (1977). Postembryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56: 110-156.
64. Sulston JE, White JG (1980). Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev Biol 78: 577-597.
65. Sundaram M (2006). RTK/Ras/MAP signaling. In: WormBook (ed). The C. elegans Research Community WormBook, doi/10.1895/wormbook.1.80.1, http://www.wormbook.org.
66. van Nimwegen E, Crutchfield JP, Huynen M (1999). Neutral evolution of mutational robustness. Proc Natl Acad Sci USA 96: 9716-9720.
67. Vassilieva LL, Hook AM, Lynch M (2000). The fitness effects of spontaneous mutations in Caenorhabditis elegans. Evolution 54: 1234-1246.
68. von Dassow G, Meir E, Munro EM, Odell GM (2000). The segment polarity network is a robust developmental module. Nature 406: 188-192.
69. Waddington CH (1942). Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
70. Wagner A (1996). Does evolutionary plasticity evolve? Evolution 50: 1008-1023.
71. Wagner A (2000). The role of population size, pleiotropy and fitness effects of mutations in the evolution of overlapping gene functions. Genetics 154: 1389-1401.
72. Wagner A (2005a). Robustness and Evolvability in Living Systems. Princeton University Press: Princeton and Oxford. p 367.
73. Wagner A (2005b). Robustness, evolvability, and neutrality. FEBS Lett 579: 1772-1778.
74. Wagner A (2005c). Distributed robustness versus redundancy as causes of mutational robustness. Bioessays 27: 176-188.
75. Wagner GP, Booth G, Bagheri-Chaichian H (1997a). A population genetic theory of canalization. Evolution 51: 329-347.
76. Wagner GP, Laublicher MD, Bagheri-Chaichian H (1997b). Genetic measurement theory of epistatic effects. Genetica 103: 569-580.
77. Wilke CO (2001). Adaptive evolution on neutral networks. Bull Math Biol 63: 715-730.
78. Yoo AS, Bais C, Greenwald I (2004). Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development. Science 303: 663-666.
79. Yoon CH, Lee J, Jongeward GD, Sternberg PW (1995). Similarity of sli-1, a regulator of vulval development in Caenorhabditis elegans, to the mammalian proto-oncogene, c-cbl. Science 269: 1102-1105.