Bacterial endosymionts in bat flies (Diptera: Hippoboscoidea: Streblidae and Nycteribiidae)
Morse, Solon F.
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Many obligate hematophagous arthropods have formed associations with bacterial symbionts. These associates are thought to provide essential nutrients that are lacking in their host's blood diet. Due to their intimate association with vertebrates, obligate blood feeders may also serve as reservoirs and vectors for vertebrate pathogens. Despite the diversity and potential human health impacts of these arthropods, their bacterial associations remain poorly understood. To expand our knowledge of bacterial associates in bat flies, this study focused on the diversity and evolution of bacterial symbionts in a global sampling of six nominal subfamilies of bat flies (Streblidae and Nycteribiidae), which are obligate hematophagous parasites of bats. Results identified an array of obligate and facultative associations, which may function in symbiotic as well as pathogenic relationships. Phylogenetic analysis identified four independent invasions of distantly related gammaproteobacterial lineages throughout bat fly evolution, including two novel symbiont lineages, and extended the geographic and taxonomic range of a previously recognized lineage. While overall bacterial phylogenies showed little congruence with the phylogenies of their hosts, symbiont-host co-divergence is apparent within some reciprocally monophyletic subclades. In addition, several bat fly genera were associated with widely distributed insect-associated Arsenophonus spp.; these associations may represent symbiont replacement events and/or local transient infections. The detection of symbionts in fly pupae suggests vertical transmission in both novel bacterial clades, while in situ hybridization identified bacteriome localization in very different anatomical regions within the fly host's body for two clades (Trichobiinae and Nycterophiliinae). One of the novel monophyletic clades of Gammaproteobacteria detected in bat flies occurs in the small, poorly known streblid genus Nycterophilia, sampled across a wide geographic distribution, and is only distantly related to symbionts found in other bat fly genera. While its specific function in Nycterophilia remains unknown, high symbiont prevalence in adult flies, vertical transmission between generations, general co-divergence between hosts and symbionts, and high AT composition bias in symbiont genes taken together suggest that this host-symbiont association is both ancient and obligatory. That Nycterophilia contains a unique bacterial clade suggests an endosymbiont replacement event. This replacement is discussed in the context of Nycterophilia ecology, and results suggest that ecological factors beyond trophic niche may influence host-symbiont evolutionary dynamics. A large number of novel Bartonella lineages (Alphaproteobacteria) were detected in a wide geographic sampljng of bat fly species belonging to both families (Nycteribiidae and Streblidae). Bartonellae are facultatively intracellular bacteria, and are often assumed to be silent pathogens, forming asymptomatic, persistent bacteraemia in reservoir host species. In wildlife, including bats, little evidence for pathogenicity exists, although this may be due to the lack of syndromic reporting in wildlife disease surveillance. Their ubiquitous presence in bat flies suggests a role as reservoirs for bat Bartonella. Phylogenetic analyses point to a potentially early association with bat flies in the bacterial lineage's evolutionary history. A subset of fly associated bartonellae seems to have radiated with bat flies and their hosts. Bacterial clades detected in both fly and bat hosts suggest that the flies might act as competent vectors for Bartonella, while vertical transmission between generations intimates that, in addition to the pathogenic phenotype, some Bartonella may display parasitic or mutualistic phenotypes.