Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila

Abstract

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.

Enteric bacterial infection inDrosophilainduces whole-body alterations in metabolic gene expression independently of the Immune Deficiency (Imd) signalling pathway

“…2020; K im et al . 2021; S adanandappa et al . 2021), it is possible that they may modulate either process to help promote infection tolerance.…”

Enteric bacterial infection in Drosophila induces whole-body alterations in metabolic gene expression independently of the immune deficiency signaling pathway

“…It is known that infected flies will alter their feeding behavior, often to avoid eating infected food ( Soldano et al 2016 ; Charroux et al 2020 ; Cai et al 2021 ), and they will alter their fecundity and egg-laying behavior ( Masuzzo et al 2019 , 2020 ), perhaps to limit the energetically costly process of reproduction while fighting infection ( Schwenke et al 2016 ). Given that several of the neuropeptide signaling molecules and pathways that we see downregulated upon infection are known to affect both feeding and reproduction ( Schoofs et al 2017 ; Ameku et al 2018 ; Nassel and Zandawala 2019 ; Hadjieconomou et al 2020 ; Kim et al 2021 ; Sadanandappa et al 2021 ), it is possible that they may modulate either process to help promote infection tolerance. Thus, enteric infection-mediated changes in both gut-to-brain signaling and CNS signaling may be a general mechanism to coordinate multiple whole-body physiological and behavioral responses to infection.…”

Impact of Microorganisms and Parasites on Neuronally Controlled Drosophila Behaviours

“…First, the sight and smell of wasps causes a rapid decline in oviposition through egg retention, coupled with apoptosis via effector caspases at a specific stage of oogenesis [ 70 , 72 ]. These parasitoid-induced changes in germ cell development are induced by suppression of neuropeptide F (NPF) signaling in the brain, which occurs following the sight of wasps [ 73 , 74 ]. The oviposition depression is triggered when the fly sees the wasp.…”