Drosophila larvae and pupae are at high risk of parasitoid infection in nature. To circumvent parasitic stress, fruit flies have developed various survival strategies, including cellular and behavioral defenses. We show that adult Drosophila females exposed to the parasitic wasps, Leptopilina boulardi , decrease their total egg-lay by deploying at least two strategies: Retention of fully developed follicles reduces the number of eggs laid, while induction of caspase-mediated apoptosis eliminates the vitellogenic follicles. These reproductive defense strategies require both visual and olfactory cues, but not the MB247 -positive mushroom body neuronal function, suggesting a novel mode of sensory integration mediates reduced egg-laying in the presence of a parasitoid. We further show that neuropeptide F (NPF) signaling is necessary for both retaining matured follicles and activating apoptosis in vitellogenic follicles. Whereas previous studies have found that gut-derived NPF controls germ stem cell proliferation, we show that sensory-induced changes in germ cell development specifically require brain-derived NPF signaling, which recruits a subset of NPFR-expressing cell-types that control follicle development and retention. Importantly, we found that reduced egg-lay behavior is specific to parasitic wasps that infect the developing Drosophila larvae, but not the pupae. Our findings demonstrate that female fruit flies use multimodal sensory integration and neuroendocrine signaling via NPF to engage in parasite-specific cellular and behavioral survival strategies. Author summary Behavioral adaptation to environmental threats such as infectious diseases or predators increases the survival and fitness of an organism. Here, we studied behavioral immunity in adult Drosophila females that protect their progeny from the parasitic infection. We show that Drosophila females modify their oviposition behavior in the presence of a parasitic wasp. This change in reproductive behavior is highly specific to Leptopilina wasps, which necessitates both visual as well as the parasitoid-specific olfactory cues. In addition, we find that the transient retention of matured follicles and increased apoptosis of the developing follicles in the parasitoid-exposed Drosophila ovaries results in an egg-lay reduction. We also identify that the neuroendocrine signaling involving neuropeptide F (NPF) and its cognate receptor, NPFR, mediates the parasitoid-induced egg-lay depression and germline physiological modifications. Based on the innate recognition of the predatory threat, our study unravels the cellular and physiological mechanisms that underlie an ecological relevant form of behavioral adaptation in Drosophila .
【초록키워드】 Apoptosis, Infectious diseases, Depression, Stress, Immunity, Infection, Infectious disease, survival, retention, female, Control, fitness, receptor, neuroendocrine, caspase, cellular, Signaling, olfactory, physiological, cell proliferation, high risk, stem cell, germ cell, reduction, Drosophila, Previous studies, physiological mechanism, Author, germline, organism, modifications, previous study, Defense, parasitoid, progeny, infect, Cell, decrease, PROTECT, neuronal function, identify, addition, reduced, increase, changes in, reduce, circumvent, subset, reproductive, activating, modify, ecological, engage, underlie, environmental threat, predatory, recruit, 【제목키워드】 Signaling, regulate, Neuropeptide,