The follicular epithelium (FE) in the Drosophila melanogaster ovary is an excellent model system to study epithelial processes and behaviors, such as cell-cell communication, cell cycle regulation, and epithelial morphogenesis. The growth and morphogenesis of the FE is closely coordinated with the oocyte via cell-cell communication, similar to how epithelial-mesenchymal interactions drive vertebrate tissue development. The FE in the genetically tractable Drosophila system is therefore an excellent model for the study of vertebrate epithelial behaviors such as growth regulation, morphogenesis, tissue homeostasis, as well as tumorigenesis and metastasis. The focus of the research here is the characterization of non-typical epithelial behaviors in the Drosophila FE using cell- and tissue-specific genetic manipulation and confocal microscopy. In the first part of this thesis, I present a detailed characterization of a novel non-typical epithelial process in the FE termed ‘patency’, characterized by the transient opening of intercellular spaces between follicle cells that could assist in the trans-epithelial transport of lipids across the FE. Images from Immunostaining and transmission electron microscopy (TEM) revealed that during mid-vitellogenesis, tricellular contacts between follicle cells open and create transient channels across the entire epithelial monolayer. I found consistent temporal and spatial patterns of patency in the Drosophila FE. I also show that the transcription factor Ttk69 restricts the temporal range of patency, and the underlying dorsal-anterior signals which use the Epithelial growth factor receptor (EGFR) and Decapentaplegic (Dpp) ligand influence the spatial pattern of patency. Together, the data from this study show that patency is a novel epithelial property in a classic model system, highlighting the use of the FE as a model to study conserved epithelial processes such as tricellular junction dynamics, and trans-epithelial transport. Development of the Drosophila FE is also controlled by growth regulatory pathways that couple nutrient availability to development and regulate cell growth. In the second part of my thesis, using the Drosophila follicle cell system, I investigated the effects of inducing differential growth in the endocycling cells. I show by mosaic analysis that induction of higher growth rate in a subset of endocycling follicle cells results in a non-autonomous response which is characterized by smaller wild-type cells of the epithelium in response to this induced differential growth. Here, we termed this non-typical epithelial response Non-autonomous Cellular Compaction (NCC), wherein the wildtype cells are reduced in size, instead of undergoing overcrowding-induced extrusion from the epithelial monolayer. The NCC cells present lower cell and nuclear volumes, as well as reduced protein synthesis rates, potentially in response to lower levels of activation of the insulin pathway. We found using FACS analysis and confocal microscopy that the DNA content in the NCC cells is not altered, indicating that the rate of endocycling is maintained. Overall, our data reveals a non-autonomous, non-typical epithelial response to differential growth involving cell size plasticity in the endocycling FE. Most mammalian tissues are highly heterogeneous in nature, and the study of non-autonomous effects such as NCC have both scientific and medical significance. Complementary to NCC, a non-autonomous increase in cell size has been previously reported in response to a local loss of tissue volume in the endocycling Drosophila FE, a process called compensatory cellular hypertrophy or CCH. A model was proposed, involving the recruitment of mechanotransducers for the increased growth of the CCH cells. In the last part of my research, I explored the roles of a mechanotransducer, No mechanoreceptor potential C (NompC), previously identified from a screen, for regulating growth of the endocycling follicle cells to generate CCH. Using mosaic analysis in the endocycling epithelium, I show that NompC does not appear to have a direct role in the growth of the epithelial cells, but affects other epithelial properties such as nuclear placement within the cells. This study reveals that the CCH response may indeed be more complex and involve multiple mechanotransducers. Overall, my research characterizes a set of non-typical epithelial behaviors in the classic Drosophila melanogaster FE model, including patency for oocyte lipid uptake, and non-autonomous cell size plasticity, NCC, in response to differential growth in the endocycling FE. This study creates a platform for further research into conserved epithelial behavior, trans-epithelial transport mechanisms, non-autonomous growth regulation, and cell size plasticity, as well as providing a broader characterization of the widely used FE model system. Together, the epithelial properties highlighted in my research now makes these non-typical epithelial behaviors accessible for genetic dissection, presenting the Drosophila FE as a model to study various vertebrate disease states that share these epithelial properties.