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The Drosophila eggshell constitutes a remarkable system for the study of epithelial patterning, both experimentally and through computational modeling. Dorsal eggshell appendages arise from specific regions in the anterior follicular epithelium that covers the oocyte: two groups of cells expressing broad (roof cells) bordered by rhomboid expressing cells (floor cells). Despite the large number of genes known to participate in defining these domains and the important modeling efforts put into this developmental system, key patterning events still lack a proper mechanistic understanding and/or genetic basis, and the literature appears to conflict on some crucial points. We tackle these issues with an original, discrete framework that considers single-cell models that are integrated to construct epithelial models. We first build a phenomenological model that reproduces wild type follicular epithelial patterns, confirming EGF and BMP signaling input as sufficient to establish the major features of this patterning system within the anterior domain. Importantly, this simple model predicts an instructive juxtacrine signal linking the roof and floor domains. To explore this prediction, we define a mechanistic model that integrates the combined effects of cellular genetic networks, cell communication and network adjustment through developmental events. Moreover, we focus on the anterior competence region, and postulate that early BMP signaling participates with early EGF signaling in its specification. This model accurately simulates wild type pattern formation and is able to reproduce, with unprecedented level of precision and completeness, various published gain-of-function and loss-of-function experiments, including perturbations of the BMP pathway previously seen as conflicting results. The result is a coherent model built upon rules that may be generalized to other epithelia and developmental systems.

Background: Morphological innovation is an elusive and fascinating concept in evolutionary biology. A novel structure may open up an array of possibilities for adaptation, and thus is fundamental to the evolution of complex multicellular life. We use the respiratory appendages on the dorsal-anterior side of the Drosophila eggshell as a model system for morphological novelty. To study the co-option of genetic pathways in the evolution of this novelty we have compared oogenesis and eggshell patterning in Drosophila melanogaster with Ceratitis capitata, a dipteran whose eggs do not bear dorsal appendages., Results: During the final stages of oogenesis, the appendages are formed by specific groups of cells in the follicular epithelium of the egg chamber. These cells are defined via signaling activity of the Dpp and EGFr pathways, and we find that both pathways are active in C. capitata oogenesis. The transcription factor gene mirror is expressed downstream of EGFr activation in a dorsolateral domain in the D. melanogaster egg chamber, but could not be detected during C. capitata oogenesis. In D. melanogaster, mirror regulates the expression of two important genes: broad, which defines the appendage primordia, and pipe, involved in embryonic dorsoventral polarity. In C. capitata, broad remains expressed ubiquitously throughout the follicular epithelium, and is not restricted to the appendage primordia. Interestingly pipe expression did not differ between the two species., Conclusions: Our analysis identifies both broad and mirror as important nodes that have been redeployed in the Drosophila egg chamber patterning network in the evolution of a morphologically novel feature. Further, our results show how pre-existing signals can provide an epithelium with a spatial coordinate system, which can be co-opted for novel patterns.