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Almost all animals possess microbial gut communities, but the nature of these communities varies immensely. For example, in social bees and mammals, composition is relatively constant within species and dominated by specialist bacteria that do not live elsewhere; whereas, in laboratory studies and field surveys of Drosophila melanogaster, gut communities consist of bacteria that are ingested with food and that vary widely among individuals and localities. We addressed whether an ecological specialist in its natural habitat has a microbiota dominated by gut specialists or by environmental bacteria. Drosophila nigrospiracula is a Sonoran Desert endemic restricted to decaying tissues of two giant columnar cacti, Pachycereus pringlei (cardón) and Carnegeia gigantea (saguaro). We found that the D. nigrospiracula microbiota differs strikingly from that of the cactus tissue on which the same flies feed. The most abundant bacteria in the flies are rare or completely absent in the cactus tissue and are consistently abundant in flies from different cacti and localities. Several of these fly-associated bacterial groups, such as the bacterial order Orbales and the genera Serpens and Dysgonomonas, have been identified in prior surveys of insects from the orders Hymenoptera, Coleoptera, Lepidoptera, and Diptera, including several Drosophila species. Although functions of these bacterial groups are mostly unexplored, Orbales species studied in bees are known to breakdown plant polysaccharides and use resulting sugars. Thus, these bacterial groups appear to be specialized to the insect gut environment, where they may colonize by direct host-to-host transmission in natural settings.Importance Flies in the genus Drosophila have become laboratory models for microbiota research, yet the bacteria commonly used in these experiments are rarely found in wild-caught flies and instead represent bacteria also present in the food. This study shows that an ecologically specialized Drosophila species possesses a distinctive microbiome, composed of bacterial types absent from their natural food but widespread in other wild-caught insects. This study highlights the importance of fieldwork-informed microbiota research.

A Distinctive and Host-Restricted Gut Microbiota in Populations of a Cactophilic Drosophila Species