Implications of changes in network size in response to environment
Bacteria with high betweenness centrality may act as hub species that maintain the stability of a network (Röttjers & Faust, 2018). In large fragments, Arsenophonus , Wolbachia , and Bartonellahad high betweenness centrality, but these bacterial taxa were less central to the networks from small fragments despite maintaining high relative abundance in flies at these sites (Figures 2 and 6). IfArsenophonus and Wolbachia are acting as primary symbionts, decreasing betweenness centrality may be indicative of changing symbiont-host interactions in response to microbiome community perturbations. The primary symbionts of blood-feeding insects play an important role in vector competence in insects (Weiss & Aksoy, 2011). For example, in tsetse flies, primary bacterial endosymbionts in the genus Wigglesworthia impede the invasion of trypanosome parasites by assisting host defenses and subsequently decrease the competence of tsetse flies to vector these harmful parasites to downstream hosts including humans (Weiss et al. 2013). As bat flies are important arthropod vectors of bat pathogens, changes in the structure of their microbiomes in response to habitat fragmentation may have implications for the disease ecology of arthropod vectored pathogens in bats.
Modules may delimit groups of bacteria with specific functional specializations and/or groups that respond in similar ways to environmental variables (Röttjers & Faust, 2018). Higher modularity may protect a community of free-living organisms from invading pathogens, because a pathogen would be isolated to one module within the community (i.e., diversity-stability debate; (Krause et al., 2003; Stouffer & Bascompte, 2010)). This hypothesis may be applicable to bacterial networks if pathogens are limited in transmission by direct competition with endogenous bacteria. However, high modularity in bacterial interaction networks may also reflect the absence of microbiome-mediated host defenses against pathogen invasion. If we revisit the tsetse fly example above, Wigglesworthia and trypanosome parasites would share an edge in a microbe interaction network becauseWigglesworthia abundance and prevalence is associated with low trypanosome abundance and prevalence mediated by host defenses. The absence of this interaction in a network might indicate thatWigglesworthia -induced host response to trypanosome invasion is impaired by other microbes in the network (e.g., priority effects) or other aspects of host health. Trypanosome transmission would be less regulated in this instance, but modularity would be high as long as trypanosome abundance and prevalence did not lead to changes in the abundance or prevalence of other microbes. In the case of bat flies, the consequences of more isolated modules for the functionality and stability of the microbiome are unclear and merit future investigation.
Our research builds upon previous evidence that the environment influences microbiome composition in addition to host factors (Amato et al., 2013; Avena et al., 2016; Becker et al., 2017; Ingala et al., 2019). However, all previous studies on the impact of the environment on microbiome composition have been conducted on free-living organisms. The interactions of bat flies with the broader environment are filtered through their obligate associations with host bats, yet the signal of environmental change is detected in the composition of bat fly microbiomes. This indicates that environmental degradation may have community-wide implications for the composition of microbiomes in various organisms, possibly through microclimatic changes that alter the pool of bacteria available in habitat patches.