Gut microbiota composition in the sympatric and diet-sharing Drosophila simulans and Dicranocephalus wallichii bowringi shaped largely by community assembly processes rather than regional species pool

Abstract

Clarifying the mechanisms underlying microbial community assembly from regional microbial pools is a central issue of microbial ecology, but remains largely unexplored. Here, we investigated the gut bacterial and fungal microbiome assembly processes and potential sources in Drosophila simulans and Dicranocephalus wallichii bowringi, two wild, sympatric insect species that share a common diet of waxberry. While some convergence was observed, the diversity, composition, and network structure of the gut microbiota significantly differed between these two host species. Null model analyses revealed that stochastic processes (e.g., drift, dispersal limitation) play a principal role in determining gut microbiota from both hosts. However, the strength of each ecological process varied with the host species. Furthermore, the source-tracking analysis showed that only a minority of gut microbiota within D. simulans and D. wallichii bowringi are drawn from a regional microbial pool from waxberries, leaves, or soil. Results from function prediction implied that host species-specific gut microbiota might arise partly through host functional requirement and specific selection across host-microbiota coevolution. In conclusion, our findings uncover the importance of community assembly processes over regional microbial pools in shaping sympatric insect gut microbiome structure and function.

Keywords: Dicranocephalus wallichii bowringi; Drosophila simulans; community assembly; gut microbiota; microbial source‐tracking.

Figure 1

Diversity and structure of microbial communities in D. simulans, D. wallichii bowringi, waxberry, leaves, and soil. Box and whisker plots of three α‐diversity indices (Pielou evenness, Richness, and Shannon diversity index) of bacterial (A) and fungal (B) communities in each group. Different letters above the whiskers denote significant differences between each group determined with analysis of variance tests (p < 0.05). Nonmetric multidimensional scaling (NMDS) of bacterial (C) and fungal (D) communities, with clustering based on Bray–Curtis similarities. Relative abundances of bacterial genera (E) and fungal genera (F) in microbial composition among D. simulans, D. wallichii bowringi, waxberry, leaves, and soil.

Figure 2

Co‐occurrence networks of gut bacteria and fungi in D. wallichii bowringi (A) and D. simulans (B). Edges represent statistically significant Spearman correlations (ρ > |0.6|, p < 0.05), whereas blue and red lines, respectively, indicate significant positive and negative correlations. Relative abundances of OTUs in each microbial community are represented by the sizes of the points.

Figure 3

Potential sources of gut bacteria (A) and fungi (B) in the two wild, sympatric insect species. Numbers next to arrows indicate the proportion of the fly D. simulans and beetle D. wallichii bowringi microbes potentially derived primarily from the microbiota of their diet waxberry or surrounding leaves and soil.

Figure 4

Mechanisms of microbial community assembly in D. wallichii bowringi, D. simulans, waxberry, leaves, and soil. Box and whisker plots of contributions of deterministic (|βNTI| ≥ 2) and stochastic processes (|βNTI| < 2) on bacterial (A) and fungal (B) community assembly in each group. The relative contributions of ecological processes in driving the bacterial (C) and fungal (D) assembly in each group.

Figure 5

Functional predictions of bacteria and fungi varied among different sample types. Nonmetric multidimensional scaling ordination (NMDS) showing that potential functions of the bacteria (A) and fungi (C) clustered by sample type using Bray–Curtis dissimilarity distance. Boxplots representing significantly different potential functions of the bacteria (B) and fungi (D) between D. simulans and D. wallichii bowringi. The negative log2 of adjusted p values plotted against the logFC between D. simulans and D. wallichii bowringi. Red, blue and gray dots indicate the enriched, depleted, and nonsignificant functional categories, respectively. Detailed information for these functional categories are in the Supporting Information: Table S5.

Figure 6

An illustration of the sources and assembly of microbiota associated with the gut of D. simulans and D. wallichii bowringi and the regional pool of microbiomes in the external environment (e.g., waxberry, leaf, and soil) that they may draw from. Shapes represent different types of microbes. Different arrows indicate the extent of each factor in shaping the microbial community: solid arrows indicate a strong effect, while two types of dotted arrows show a weak effect or inferred effect.