Fruit fly phylogeny imprints bacterial gut microbiota

Abstract

One promising avenue for reconciling the goals of crop production and ecosystem preservation consists in the manipulation of beneficial biotic interactions, such as between insects and microbes. Insect gut microbiota can affect host fitness by contributing to development, host immunity, nutrition or behavior. However, the determinants of gut microbiota composition and structure, including host phylogeny and host ecology, remain poorly known. Here we used a well-studied community of eight sympatric fuit fly species to test the contributions of fly phylogeny, fly specialization, and fly sampling environment on the composition and structure of bacterial gut microbiota. Comprising both specialists and generalists, these species belong to five genera belonging to two tribes of the Tephritidae family. For each fly species, one field and one laboratory samples were studied. Bacterial inventories to the genus level were produced using 16S metabarcoding with the Oxford Nanopore technology. Sample bacterial compositions were analyzed with recent network-based clustering techniques. Whereas gut microbiota were dominated by the Enterobacteriacaeae family in all samples, microbial profiles varied across samples, mainly in relation with fly identity and sampling environment. Alpha diversity varied across samples and was higher in the Dacinae tribe than in the Ceratitinae tribe. Network analyses allowed grouping samples according to their microbial profiles. The resulting groups were very congruent with fly phylogeny, with a significant modulation of sampling environment, and a very low impact of fly specialization. Such a strong imprint of host phylogeny in sympatric fly species, some of which share much of their host plants, suggests important control of fruit flies on their gut microbiota through vertical transmission and/or intense filtering of environmental bacteria.