Fetal programming: Masculinization increases daughter lifetime reproduction at high competition

Abstract High testosterone along with masculinized traits is often considered maladaptive for female mammals, based on clinical cases of reproductive disorders and standardized animal studies. Yet, despotic species, where masculinized females dominate reproduction, challenge this view. Here, we provide support for selective benefits of female masculinization, by applying the fetal programming hypothesis. Using long-term data on free-ranging house mice exposed to naturally fluctuating densities signaling reproductive competition, we show that high-testosterone mothers produced masculinized daughters with elongated anogenital distance who achieved higher lifetime reproductive success under high-density conditions. However, population-level female testosterone and daughter masculinization declined as competition intensified. Mismatching individual fitness benefits and population trends suggest masculinization is shaped by trade-offs among maternal quality, offspring demands, and ecological and social constraints. We conclude female masculinization is not inherently maladaptive but enables competitive mothers under reproductive competition providing selective benefits for daughters – a process relevant within and likely also across species.