All developmental processes rely on a complex interplay of gene regulatory network (GRN) interactions. A major challenge is to determine not only which GRNs function in a given developmental process, but also how GRNs and their interactions are modulated over evolutionary time to generate morphological variations that impact fitness and thus are subject to natural selection. We are using the developing ovary of Drosophila as a system to address these challenges. The ovary comprises a number of egg-producing structures called ovarioles, and ovariole number is positively correlated with egg-laying, making ovariole number a trait that likely impacts fitness. Ovariole number is species-specific, highly heritable and also influenced by environmental factors including nutrition. We had previously identified the Hippo signaling pathway as a major regulator of ovariole number. Here we present the results of a genetic screen aimed at uncovering new Hippo-dependent and -independent modulators of reproductive capacity. We provide evidence that all major signaling pathways impact either ovariole number or egg-laying or both, and that some of them act synergistically with Hippo signaling to do so. A network analysis of the screen phenotypes yielded three major and novel outcomes. First, we find that egg-laying and ovariole number are regulated by non-overlapping genetic modules. Second, we predict the involvement of previously untested genes in ovariole number regulation. Finally, we distinguish between genetic modules that are likely to be major “on/off” switches for reproductive capacity, and modules that are more likely to provide the “fine tuning” dials through which evolutionary change generates ovariole number variation across species.
All developmental processes rely on a complex interplay of gene regulatory network (GRN) interactions. A major challenge is to determine not only which GRNs function in a given developmental process, but also how GRNs and their interactions are modulated over evolutionary time to generate morphological variations that impact fitness and thus are subject to natural selection. We are using the developing ovary of Drosophila as a system to address these challenges. The ovary comprises a number of egg-producing structures called ovarioles, and ovariole number is positively correlated with egg-laying, making ovariole number a trait that likely impacts fitness. Ovariole number is species-specific, highly heritable and also influenced by environmental factors including nutrition. We had previously identified the Hippo signaling pathway as a major regulator of ovariole number. Here we present the results of a genetic screen aimed at uncovering new Hippo-dependent and -independent modulators of reproductive capacity. We provide evidence that all major signaling pathways impact either ovariole number or egg-laying or both, and that some of them act synergistically with Hippo signaling to do so. A network analysis of the screen phenotypes yielded three major and novel outcomes. First, we find that egg-laying and ovariole number are regulated by non-overlapping genetic modules. Second, we predict the involvement of previously untested genes in ovariole number regulation. Finally, we distinguish between genetic modules that are likely to be major “on/off” switches for reproductive capacity, and modules that are more likely to provide the “fine tuning” dials through which evolutionary change generates ovariole number variation across species.
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