Some Like It Hot: Evolution and Ecology of Novel Endosymbionts in Bat Flies of Cave-Roosting Bats (Hippoboscoidea, Nycterophiliinae)
ABSTRACTWe investigated previously unknown associations between bacterial endosymbionts and bat flies of the subfamily Nycterophiliinae (Diptera, Streblidae). Molecular analyses revealed a novel clade ofGammaproteobacteriainNycterophiliabat flies. This clade was not closely related toArsenophonus-like microbes found in its sister genusPhalconomusand other bat flies. High population infection rates inNycterophiliaacross a wide geographic area, the presence of the symbionts in pupae, the general codivergence between hosts and symbionts, and high AT composition bias in symbiont genes together suggest that this host-symbiont association is obligate in nature and ancient in origin. SomeNycterophiliasamples (14.8%) also containedWolbachiasupergroup F (Alphaproteobacteria), suggesting a facultative symbiosis. Likelihood-based ancestral character mapping revealed that, initially, obligate symbionts exhibited association with host-specificNycterophiliabat flies that use a broad temperature range of cave environments for pupal development. As this mutualism evolved, the temperature range of bat flies narrowed to an exclusive use of hot caves, which was followed by a secondary broadening of the bat flies' host associations. These results suggest that the symbiosis has influenced the environmental tolerance of parasite life history stages. Furthermore, the contingent change to an expanded host range ofNycterophiliabat flies upon narrowing the ecological niche of their developmental stages suggests that altered environmental tolerance across life history stages may be a crucial factor in shaping parasite-host relationships.