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How reproductive organs evolve is a fundamental question in biology as they play a major role in breeding success and evolution. However, our molecular understanding of gonad evolution in vertebrates is mainly restricted to mammals and remains limited due to technical barriers that were until very recently insurmountable. Consequently, it is commonly assumed that the testis is the main organ at the origin of evolutionary innovations in vertebrates, as it shows a faster evolution across mammals compared to other organs including the ovary. Based on preliminary molecular data and phenotypic observations, we propose the new hypothesis that the ovary may evolve particularly fast in teleost fishes, making it a major driver for evolutionary adaptation in half vertebrates on earth. In this context, the main goal of Evo-Ovo is to decipher the cellular and molecular origins and diversification of reproductive organs over the 300 million years of teleost fish evolution. This ambitious endeavor is timely and feasible thanks to the combination of cutting-edge multi-omics techniques and novel quantitative approaches we will develop. First, we will unravel the evolutionary plasticity and associated selective pressure across hundreds of newly available genomes using large-scale comparative genomics. Second, we will trace the cellular and molecular evolution of fish gonads by generating and comparing single-cell atlases across representative species showing divergent ovarian features. Evo-Ovo results will be key to uncover the evolution of species, reproductive organs, and genomes under a novel hypothesis. These fundamental advances will also pave the way to applied studies by providing unique resources, insights, and methods that will be useful for agriculture and medicine at large.