Suitable habitat fragment size, isolation, and distance from a source are important variables influencing community composition of plants and animals, but the role of these environmental factors in determining composition and variation of host-associated microbial communities is poorly known. In parasite-associated microbial communities, it is hypothesized that evolution and ecology of an arthropod parasite will influence its microbiome more than broader environmental factors, but this hypothesis has not been extensively tested. To examine the influence of the broader environment on the parasite microbiome, we applied high-throughput sequencing of the V4 region of 16S rRNA to characterize the microbiome of 222 obligate ectoparasitic bat flies (Streblidae and Nycteribiidae) collected from 155 bats (representing six species) from ten habitat fragments in the Atlantic Forest of Brazil. Parasite species identity is the strongest driver of microbiome composition. To a lesser extent, reduction in habitat fragment area, but not isolation, is associated with an increase in connectance and betweenness centrality of bacterial association networks driven by changes in the diversity of the parasite community. Controlling for the parasite community, bacterial network topology covaries with habitat patch area and exhibits parasite-species specific responses to environmental change. Taken together, habitat loss may have cascading consequences for communities of interacting macro- and microorgansims.  

Skin is the largest mammalian organ and the first defensive barrier against the external environment. The skin and fur of mammals can host a wide variety of ectoparasites, many of which are phylogenetically diverse, specialized, and specifically adapted to their hosts. Among hematophagous dipteran parasites, volatile organic compounds (VOCs) are known to serve as important attractants, leading parasites to compatible sources of blood meals. VOCs have been hypothesized to be mediated by host-associated bacteria, which may thereby indirectly influence parasitism. Host-associated bacteria may also influence parasitism directly, as has been observed in interactions between animal gut microbiota and malarial parasites. Hypotheses relating bacterial symbionts and eukaryotic parasitism have rarely been tested among humans and domestic animals, and have to our knowledge never been tested in wild vertebrates. In this study, we use Afrotropical bats, hematophagous ectoparasitic bat flies, and haemosporidian (malarial) parasites vectored by bat flies as a model to test the hypothesis that the vertebrate host microbiome is linked to parasitism in a wild system. We identify significant correlations between bacterial community composition of the skin and dipteran ectoparasite prevalence across four major bat lineages, as well as striking differences in skin microbial network characteristics between ectoparasitized and non-ectoparasitized bats. We also identify links between the oral microbiome and presence of malarial parasites among miniopterid bats. Our results support the hypothesis that microbial symbionts may serve as indirect mediators of parasitism among eukaryotic hosts and parasites.