Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster

Abstract

Animals are routinely colonized by microorganisms. Despite many studies documenting the microbial taxa associated with animals, the pattern and ecological determinants of among-animal variation in microbial communities are poorly understood. This study quantified the bacterial communities associated with natural populations of Drosophila melanogaster. Across five collections, each fly bore 16-78 OTUs, predominantly of the Acetobacteraceae, Lactobacillaceae, and Enterobacteriaceae. Positive relationships, mostly among related OTUs, dominated both the significant co-occurrences and co-association networks among bacteria, and OTUs with important network positions were generally of intermediate abundance and prevalence. The prevalence of most OTUs was well predicted by a neutral model suggesting that ecological drift and passive dispersal contribute significantly to microbiome composition. However, some Acetobacteraceae and Lactobacillaceae were present in more flies than predicted, indicative of superior among-fly dispersal. These taxa may be well-adapted to the Drosophila habitat from the perspective of dispersal as the principal benefit of the association to the microbial partners. Taken together, these patterns indicate that both stochastic processes and deterministic processes relating to the differential capacity for persistence in the host habitat and transmission between hosts contribute to bacterial community assembly in Drosophila melanogaster.

Fig. 1

Composition and diversity of the microbiota of individual D. melanogaster. (a) Relative abundance of bacterial orders present in individual male D. melanogaster grouped by collection. The low abundance category includes all orders that contributed <5% of the reads in that individual. The number of OTUs (b) and genera (c) detected across each evenly subsampled collection (gray bars) and the mean number of taxa (with standard deviation) in the eight randomly chosen individuals (white bars)

Fig. 2

Principal coordinates analysis (PCoA) ordinations of pairwise Jaccard distances based on the presence/absence of bacterial OTUs (a) and Bray–Curtis distances based on relative abundance of bacterial OTUs (b) between samples. Collections are represented by different shapes. The variation explained by the PCoA axes is listed in parentheses

Fig. 3

Pairwise co-occurrence patterns between the most prevalent bacterial OTUs. Each tick on the x- and y-axes refers to an OTU, ordered by family, order and phylum

Fig. 4

Co-association network of bacterial OTUs in the gut microbiota of individual male D. melanogaster. Nodes represent the 46 OTUs that are present in at least three collections. For all plots, gray edges indicate positive co-associations, red edges represent negative co-associations, and edge thickness corresponds to confidence in the association. (a) Node color represents bacterial family and node labels refer to OTU IDs from Supplementary Dataset 1d. (b) Modules based on edge betweenness are represented with convex hulls. (c) Intensity of blue color indicates greater node degree and increasing size indicates higher betweenness centrality. (d) Intensity of green color indicates greater OTU prevalence and increasing size indicates higher mean relative abundance across all individuals

Fig. 5

Characteristics of neutral models for collections of D. melanogaster. (a) Akaike information criterion (AIC) scores comparing neutral model fit to fit of a binomial model. (b) The percent of OTUs from each collection that fall above, below and within neutral model prediction. (c) Principal coordinates analysis plot of partitions above and below neutral model predictions based on Jaccard index calculated from the presence/absence of OTUs

Fig. 6

Fit of neutral model for Collection-A (a), Collection-B (b), Collection-C (c), Collection-D (d), and Collection-E (e). The predicted occurrence frequency is shown as a solid gray line and dashed lines indicate the 95% confidence interval around the neutral model prediction. Each point represents an OTU and taxa whose presence differs significantly between above and below neutral model partitions are highlighted