Abstract
Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab.
Highlights
The genetic and experimental tractability of Drosophila melanogaster often overshadows the phenotypic, evolutionary and ecological diversity of its relatives
To establish an ecological and comparative background for experimental studies, we have conducted a global survey of bacterial communities associated with natural populations of 14 species of Drosophila and related genera
Despite the taxonomic and ecological diversity of these species, we find that they are associated with the same dominant bacterial groups
Summary
The genetic and experimental tractability of Drosophila melanogaster often overshadows the phenotypic, evolutionary and ecological diversity of its relatives. Over 3000 species of Drosophila and related genera inhabit all continents except Antarctica, occur in practically every type of habitat, and show a great variety of morphological, behavioral, and life-history traits [1]. While the well-known cosmopolitan species are considered generalists, as decaying fruit of many different plants makes for an acceptable substrate, dietary specialization has evolved many times within Drosophila. Other Drosophila species use flowers, mushrooms, sap fluxes, cambium, decaying vegetation, and cacti as feeding and breeding sites [3,4]. Dietary shifts have occurred numerous times within the genus, and closely related species are known to utilize different types of food sources [5,6,7]. It is common to find phylogenetically distant species using the same food source. In almost all of these cases, the biotic environment that Drosophila are interacting with, especially the microbial communities associated with these flies, is unknown
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