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Patterning of  C .  elegans  vulval cell fates relies on inductive signaling. In this induction event, a single cell, the gonadal anchor cell, secretes LIN-3/EGF and induces three out of six competent precursor cells to acquire a vulval fate. We previously showed that this developmental system is robust to a four-fold variation in  lin-3/EGF  genetic dose. Here using single-molecule FISH, we find that the mean level of expression of  lin-3  in the anchor cell is remarkably conserved. No change in  lin-3  expression level could be detected among  C .  elegans  wild isolates and only a low level of change—less than 30%—in the  Caenorhabditis  genus and in  Oscheius tipulae . In  C .  elegans ,  lin-3  expression in the anchor cell is known to require three transcription factor binding sites, specifically two E-boxes and a nuclear-hormone-receptor (NHR) binding site. Mutation of any of these three elements in  C .  elegans  results in a dramatic decrease in  lin-3  expression. Yet only a single E-box is found in the  Drosophilae  supergroup of  Caenorhabditis  species, including  C .  angaria , while the NHR-binding site likely only evolved at the base of the  Elegans  group. We find that a transgene from  C .  angaria  bearing a single E-box is sufficient for normal expression in  C .  elegans . Even a short 58 bp  cis -regulatory fragment from  C .  angaria  with this single E-box is able to replace the three transcription factor binding sites at the endogenous  C .  elegans lin-3  locus, resulting in the wild-type expression level. Thus, regulatory evolution occurring in  cis  within a 58 bp  lin-3  fragment, results in a strict requirement for the NHR binding site and a second E-box in  C .  elegans . This single-cell, single-molecule, quantitative and functional evo-devo study demonstrates that conserved expression levels can hide extensive change in  cis -regulatory site requirements and highlights the evolution of new  cis -regulatory elements required for cell-specific gene expression.

Evolution of New cis-Regulatory Motifs Required for Cell-Specific Gene Expression in Caenorhabditis