Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis.
BACKGROUND
The Caenorhabditis vulva is formed from a row of Pn.p precursor cells, which adopt a spatial cell-fate pattern-3 degrees 3 degrees 2 degrees 1 degrees 2 degrees 3 degrees -centered on the gonadal anchor cell. This pattern is robustly specified by an intercellular signaling network including EGF/Ras induction from the anchor cell and Delta/Notch signaling between the precursor cells. It is unknown how the roles and quantitative contributions of these signaling pathways have evolved in closely related Caenorhabditis species.


RESULTS
Cryptic evolution in the network is uncovered by quantification of cell-fate-pattern frequencies obtained after displacement of the system out of its normal range, either by anchor-cell ablations or through LIN-3/EGF overexpression. Silent evolution in the Caenorhabditis genus covers a large neutral space of cell-fate patterns. Direct induction of the 1 degrees fate as in C. elegans appeared within the genus. C. briggsae displays a graded induction of 1 degrees and 2 degrees fates, with 1 degrees fate induction requiring a longer time than in C. elegans, and a reduced lateral inhibition of adjacent 1 degrees fates. C. remanei displays a strong lateral induction of 2 degrees fates relative to vulval-fate activation in the central cell. This evolution in cell-fate pattern space can be experimentally reconstituted by mild variations of Ras, Wnt, and Notch pathway activities in C. elegans and C. briggsae.


CONCLUSIONS
Quantitative evolution in the roles of graded induction by LIN-3/EGF and Notch signaling is demonstrated for the Caenorhabditis vulva signaling network. This evolutionary system biology approach provides a quantitative view of the variational properties of this biological system.
Félix
Marie-Anne
MA
Institut Jacques Monod, Centre National de la Recherche Scientifique, Universities of Paris 6 and 7, Tour 43, 2 place Jussieu , 75251 Paris cedex 05, France. felix@ijm.jussieu.fr
D000818:Animals; D005075:Biological Evolution; D019521:Body Patterning / Q000502:physiology*; D002107:Caenorhabditis / Q000196:embryology*; D029742:Caenorhabditis elegans Proteins / Q000502:physiology; D004627:Embryonic Induction / Q000502:physiology*; D004815:Epidermal Growth Factor / Q000502:physiology; D005260:Female; D015870:Gene Expression; D051880:Receptors, Notch / Q000502:physiology; D015398:Signal Transduction / Q000502:physiology*; D014844:Vulva / Q000196:embryology; D018631:ras Proteins / Q000502:physiology
D029742:Caenorhabditis elegans Proteins; D051880:Receptors, Notch; C075912:Lin-3 protein, C elegans; D004815:Epidermal Growth Factor; D018631:ras Proteins