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Journal of Biosciences

, 34:543 | Cite as

The other side of phenotypic plasticity: a developmental system that generates an invariant phenotype despite environmental variation

  • Christian Braendle
  • Marie-Anne Félix
Article

Abstract

Understanding how the environment impacts development is of central interest in developmental and evolutionary biology. On the one hand, we would like to understand how the environment induces phenotypic changes (the study of phenotypic plasticity). On the other hand, we may ask how a development system maintains a stable and precise phenotypic output despite the presence of environmental variation. We study such developmental robustness to environmental variation using vulval cell fate patterning in the nematode Caenorhabditis elegans as a study system. Here we review both mechanistic and evolutionary aspects of these studies, focusing on recently obtained experimental results. First, we present evidence indicating that vulval formation is under stabilizing selection. Second, we discusss quantitative data on the precision and variability in the output of the vulval developmental system in different environments and different genetic backgrounds. Third, we illustrate how environmental and genetic variation modulate the cellular and molecular processes underlying the formation of the vulva. Fourth, we discuss the evolutionary significance of environmental sensitivity of this developmental system.

Keywords

Caenorhabditis elegans developmental plasticity environment robustness vulval cell fate patterning 

References

  1. Ancel L W and Fontana W 2000. Plasticity, evolvability, and modularity in RNA; J. Exp. Zool. 288 242–283CrossRefPubMedGoogle Scholar
  2. Aroian R V, Lesa G M and Sternberg P W 1994 Mutations in the Caenorhabditis elegans let-23 EGFR-like gene define elements important for cell-type specificity and function; EMBO J. 13 360–366PubMedGoogle Scholar
  3. Azevedo R B, Lohaus R, Srinivasan S, Dang K K and Burch C L 2006 Sexual reproduction selects for robustness and negative epistasis in artificial gene networks; Nature (London) 440 87–90CrossRefGoogle Scholar
  4. Battu G, Hoier E F and Hajnal A 2003 The C. elegans G-proteincoupled receptor SRA-13 inhibits RAS/MAPK signaling during olfaction and vulval development; Development 130 2657–2577CrossRefGoogle Scholar
  5. Berset T, Hoier E F, Battu G, Canevascini S and Hajnal A 2001 Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development; Science 291 1055–1058CrossRefPubMedGoogle Scholar
  6. Bradshaw A D 1965 Evolutionary significance of phenotypic plasticity in plants; Adv. Genet. 13 115–154CrossRefGoogle Scholar
  7. Braendle C, and Félix M-A 2008 Plasticity and errors of a robust developmental system in different environments; Dev. Cell (in press)Google Scholar
  8. Braendle C and Flatt T 2006. A role for genetic accommodation in evolution?; BioEssays 28 868–873CrossRefPubMedGoogle Scholar
  9. Braendle C, Milloz J, and Félix M-A 2008 Mechanisms and evolution of environmental responses in Caenorhabditis elegans; Curr. Topics Dev. Biol. 80 171–207CrossRefGoogle Scholar
  10. Clark S G, Chisholm A D and Horvitz H R 1993 Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39; Cell 74 43–55CrossRefPubMedGoogle Scholar
  11. de Visser J A, Hermisson J, Wagner G P, Ancel Meyers L, Bagheri-Chaichian H, Blanchard J L, Chao L, Cheverud J M, et al. 2003 Perspective: Evolution and detection of genetic robustness; Evolution 57 1959–1972CrossRefPubMedGoogle Scholar
  12. Debat V and David P 2001 Mapping phenotypes: canalization, plasticity and developmental stability; TREE 16 555–561Google Scholar
  13. Delattre M and Félix M-A 2001 Polymorphism and evoluton of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius; Curr. Biol. 11 631–643CrossRefPubMedGoogle Scholar
  14. Dolgin E S, Félix M-A and Cutter A D 2007 Hakuna Nematoda: Genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae; Heredity 100 304–315CrossRefPubMedGoogle Scholar
  15. Eisenmann D M, Maloof J N, Simske J S, Kenyon C and Kim S K 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 3667–3680PubMedGoogle Scholar
  16. Eldar A, Dorfman R, Weiss D, Ashe H, Shilo B Z and Barkai N 2002 Robustness of the BMP morphogen gradient in Drosophila embryonic patterning; Nature (London) 419 304–308CrossRefGoogle Scholar
  17. Eldar A, Rosin D, Shilo B-Z, and Barkai N 2003 Self-enhanced ligand degradation underlies robustness of morphogen gradients; Dev. Cell 5 635–646CrossRefPubMedGoogle Scholar
  18. Félix M-A 2007 Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis; Curr. Biol. 17 103–114CrossRefPubMedGoogle Scholar
  19. Félix M-A and Wagner A 2007 Robustness and evolution: concepts, insights and challenges from a developmental model system; Heredity 100 132–140CrossRefGoogle Scholar
  20. Ferguson E and Horvitz H R 1985 Identification and characterization of 22 genes that affect the vulval cell lineages of Caenorhabditis elegans; Genetics 110 17–72PubMedGoogle Scholar
  21. Flatt T 2005 The evolutionary genetics of canalization; Q. Rev. Biol. 80 287–316CrossRefPubMedGoogle Scholar
  22. Gibson G and Dworkin I 2004 Uncovering cryptic genetic variation; Nat. Rev. Genet. 5 681–690CrossRefPubMedGoogle Scholar
  23. Gleason J E, Korswagen H C and Eisenmann D M 2002 Activation of Wnt signaling bypasses the requirement for RTK/Ras signaling during C. elegans vulval induction; Genes Dev. 16 1281–1290CrossRefPubMedGoogle Scholar
  24. Goldschmidt 1938 Physiological genetics (New York: McGraw-Hill)Google Scholar
  25. Hansen T F and Houle D 2004 Evolvability, stabilizing selection, and the problem of stasis; in Phenotypic integration: Studying the ecology and evolution of complex phenotypes (eds) M Pigliucci and K Preston (Oxford: University Press, Oxford) pp 130–150Google Scholar
  26. Horvitz H and Sternberg P 1991 Multiple intercellular signaling systems control the development of the Caenorhabditis elegans vulva; Nature (London) 351 535–541CrossRefGoogle Scholar
  27. Houchmandzadeh B, Wieschaus E and Leibler S 2002 Establishment of developmental precision and proportions in the early Drosophila embryo. Nature (London) 415 798–802Google Scholar
  28. Houle D, Morikawa B and Lynch M 1996 Comparing mutational variabilities; Genetics 143 1467–1483PubMedGoogle Scholar
  29. Katz, W S, Hill R J, Clandinin T R and Sternberg P W 1995 Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates; Cell 82 297–307CrossRefPubMedGoogle Scholar
  30. Kiontke K, Barriere A, Kolotuev I, Podbilewicz B, Sommer R J, Fitch D and Félix M-A 2007 Trends, Stasis, and Drift in the Evolution of Nematode Vulva Development; Curr. Biol. 17 1925–1937CrossRefPubMedGoogle Scholar
  31. Kitano H 2004 Biological robustness; Nat. Rev. Genet. 5 826–837CrossRefPubMedGoogle Scholar
  32. Maloof J N and Kenyon C 1998 The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling; Development 125 181–190PubMedGoogle Scholar
  33. Meiklejohn C D and Hartl D L 2002 A single mode of canalization; Trends Ecol. Evol. 17 468–473CrossRefGoogle Scholar
  34. Meir E, von Dassow G, Munro E and Odell G M 2002 Robustness, flexibility, and the role of lateral inhibition in the neurogenic network; Curr. Biol. 12 778–786CrossRefPubMedGoogle Scholar
  35. Milloz J, Duveau F and Félix M-A 2008. Intraspecific evolution of the intercellular signaling network underlying a robust developmental system; Genes Dev. (in press)Google Scholar
  36. Moghal N, Garcia L R, Khan L A, Iwasaki K and Sternberg P W 2003 Modulation of EGF receptor-mediated vulva development by the heterotrimeric G-protein Gαq and excitable cells in C. elegans; Development 130 4553–4566CrossRefPubMedGoogle Scholar
  37. Nijhout H F 1999 Control mechanisms of polyphenic development; Bioscience 49 181–192CrossRefGoogle Scholar
  38. Nijhout H F 2002 The nature of robustness in development; Bioessays 24 553–563CrossRefPubMedGoogle Scholar
  39. Pigliucci M 2001 Phenotypic plasticity: beyond nature and nurture (Baltimore: Johns Hopkins University Press)Google Scholar
  40. Scheiner S 1993 Genetics and evolution of phenotypic plasticity; Annu. Rev. Ecol. Syst. 24 35–68CrossRefGoogle Scholar
  41. Schmalhausen I I 1949 Factors of evolution (Philadelphia, PA: Blakiston)Google Scholar
  42. Siegal M L and Bergman A 2002 Waddington’s canalization revisited: developmental stability and evolution; Proc. Natl Acad. Sci. USA 99 10528–10532CrossRefPubMedGoogle Scholar
  43. Stearns S C 1989 The evolutionary significance of phenotypic plasticity; BioScience 39 436–445CrossRefGoogle Scholar
  44. Sternberg P W 2005 Vulval development, Wormbook (ed. The C. elegans Research Community), pp. doi/10.1895/wormbook.1.6.1Google Scholar
  45. Sternberg P W and Horvitz H R 1986 Pattern formation during vulval development in Caenorhabditis elegans; Cell 44 761–772CrossRefPubMedGoogle Scholar
  46. Sulston J and Horvitz H R 1977 Postembryonic cell lineages of the nematode Caenorhabditis elegans; Dev. Biol. 56 110–156CrossRefPubMedGoogle Scholar
  47. Sulston J and White J 1980 Regulation and cell autonomy during postembryonic development of C. elegans; Dev. Biol. 78 577–597CrossRefPubMedGoogle Scholar
  48. Sultan S E 1992 Phenotypic plasticity and the neo-darwinian legacy; Evol. Trends Plants 6 61–71Google Scholar
  49. Surkova S, Kosman D, Kozlov K, Manu, Myasnikova E, Samsonova A A,. Spirov A, Vanario-Alonso C E, Samsonova M and Reinitz J 2008 Characterization of the Drosophila segment determination morphome; Dev. Biol. 313 844–862CrossRefPubMedGoogle Scholar
  50. True J R and Haag E S 2001 Developmental system drift and flexibility in evolutionary trajectories; Evol. Dev. 3 109–119CrossRefPubMedGoogle Scholar
  51. Vassilieva L L and Lynch M 1999 The rate of spontaneous mutation for life-history traits in Caenorhabditis elegans; Genetics 151 119–129PubMedGoogle Scholar
  52. von Dassow G, Meir E, Munro E M and Odell G M 2000 The segment polarity network is a robust developmental module; Nature (London) 406 188–192CrossRefGoogle Scholar
  53. Waddington C H 1942 Canalization of development and the inheritance of acquired characters; Nature (London) 150 563–565CrossRefGoogle Scholar
  54. Wagmaister J A, Gleason J E and Eisenmann D M 2006 Transcriptional upregulation of the C. elegans Hox gene lin-39 during vulval cell fate specification; Mech. Dev. 123 135–150CrossRefPubMedGoogle Scholar
  55. Wagner A 2005 Robustness and evolvability in living systems (Princeton, Oxford: Princeton University Press)Google Scholar
  56. West-Eberhard M J 1989 Phenotypic plasticity and the origins of diversity; Annu. Rev. Ecol. Syst. 20 249–278CrossRefGoogle Scholar
  57. West-Eberhard M J 2003 Developmental plasticity and evolution (Oxford: Oxford University Press)Google Scholar
  58. Yoo A S, Bais C and Greenwald I 2004 Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development; Science 303 663–666CrossRefPubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2009

Authors and Affiliations

  1. 1.Institut Jacques MonodParis cedex 05France

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