Context-dependent symbionts shape Drosophila melanogaster developmental ecology

Insects, like many other organisms, live in complex interactions with microbial symbionts that play critical roles in their ecology and evolution. These symbionts, collectively referred to as microbiota, can include bacteria, fungi, and viruses, and they influence host physiology, immunity, and nutrition. While some symbionts are transmitted vertically from parent to offspring, others are acquired from the environment, leading to transient associations. These transient microbiota are often overlooked in studies of symbiosis, which tend to focus on highly mutualistic and stable interactions. However, recent advances in sequencing technologies have revealed the ubiquity and functional importance of transient microbes, particularly in insects that breed in ephemeral resource patches (ERPs). These environments, characterized by rapidly changing resource availability, exert selection pressure upon host and microbiota in symbiosis. This thesis investigates the role of context-dependent microbiota in shaping the developmental ecology of the fruit fly Drosophila melanogaster, as a model for insects breeding in ERPs. The study aims to elucidate how environmental factors, such as substrate type, influence microbiota composition and, in turn, affect host developmental phenotypes and interactions with other organisms. By experimentally manipulating microbiota and substrate combinations, this research provides insights into the adaptive role of transient microbiota under changing environmental conditions. To achieve the study's objectives, a microcosm setup was developed to rear field-collected microbiota in association with D. melanogaster in a laboratory culture. D. melanogaster seed microbiota around oviposition sites in droplets of fecal material. I collected these microbiota on a variety of different fruits and vegetables brought out as baits. Flies reared under laboratory conditions, could associate with these field-collected and diverse microbiota. Substrates offered as oviposition site for the next fly generation act as an environmental filter for the microbiota. Finally, freshly eclosed flies pick up the microbes again from the substrate thus completing the cycle. For the first chapter I set up several microcosms in this way based on different fruit and vegetable types. The study demonstrates that the local environmental context, specifically the type of fruit, shapes the composition of bacterial and fungal symbiont communities associated with D. melanogaster. I found only few microbial species that would prevail in all environmental contexts emphasizing the importance of transient microbiota for D. melanogaster. Chapter two, the central chapter of this thesis, explores the interplay between microbiota, substrate type, and host developmental phenotypes. By experimentally mixing microbiota and substrate types, the study shows that both allochthonous (foreign) and autochthonous (native) microbiota can promote fly development. These effects are linked to the nutritive routing of essential amino acids, demonstrating that context-dependent microbiota interactions can optimize resource exploitation. However, the study also reveals that ephemeral resource patches may lead to variable partner quality and reduced mutualistic dependence, increasing ecological variability. The third chapter introduces non-insect associates, as another layer of ecological complexity. I explore the fly microbiota interaction in the presence of the phoretic nematode Panagrellus redivivoides. The nematode exerted neutral to beneficial effects on developing D. melanogaster, depending on the fruit substrate type on which the two species interacted. The final chapter examines how D. melanogaster microbiota influence the development of parasitoid wasps, at the next higher trophic level. Wasps’ reproductive success is influenced by the ecological context of the fly larvae, comprised of substrate and specific fly microbiota. While host mortality remained unaffected parasitoid success was higher in ecological contexts that previously - in the absence of the predator- produced less beneficial fly developmental phenotypes. The fly microbiota, it seems, have opposite effects on the two trophic levels. This thesis provides compelling evidence for the adaptive role of context-dependent microbiota in shaping the developmental ecology of Drosophila melanogaster. The findings demonstrate that transient microbiota can optimize resource exploitation and influence interactions with other organisms, such as parasitoids. Functionally diverse microbiota can buffer against biotic and abiotic stressors, potentially enhancing species resilience under global change. The results of this thesis emphasize the importance of integrating microbiota diversity into biodiversity studies and conservation efforts. Furthermore, they call for a greater focus on traits related to host-microbiota interactions, such as transmission routes, life-history aspects, and physiological mechanisms for microbial management. Drosophila melanogaster, as a tractable model system, offers unique opportunities to study the eco-evolutionary dynamics of symbiosis in insects and beyond. Ultimately, this research underscores the profound evolutionary implications of context-dependent host-microbiota interactions and their role in shaping the diversity of life.