Against all odds: explaining high host specificity in dispersal-prone parasites

Host specificity gauges the degree to which a parasite occurs in association with a single host species. The measure is indicative of properties of the host and parasite, as well as their ecological and co-evolutionary relationships. Host specificity is influenced by the behavior and ecology of both parasite and host. Where parasites are active, vagile and coupled with hosts whose behavior and ecology brings the parasite into contact with many potential hosts, the likelihood of host switching is increased, usually leading to lowered specificity. Bat flies are specialized, blood-feeding ectoparasites of bats worldwide. In the bat fly - bat system, numerous properties interrupt the linkage of parasite to host and should decrease specificity. For bat flies these include high levels of activity, proclivity to abandon a disturbed host, the ability to fly, and a life-history strategy that includes a pupal stage decoupled from the host. For bats these include rapid, frequent and wide-ranging flight, high species richness encouraging inter-specific encounters during foraging, roosting and reproductive events, the utilization of large, durable roosting structures that are often shared with other bat species, and utilization of common entrance/exit flyways. The biological and ecological characteristics of bats and flies should together facilitate interspecific host transfers and, over time, lead to non-specific host-parasite associations. Large surveys of Neotropical mammals and parasites, designed to eliminate artifactual host-to-host parasite transfers, unequivocally demonstrate the high host specificity of bat flies. High degrees of specificity are remarkable in light of myriad host and parasite characteristics that ought to break down such specificity. Although host-specific parasites often have limited dispersal capability, this is not the case for some groups, including active, mobile bat flies. Host specificity in parasites with high dispersal capability is likely related to adaptive constraints. Among these may be a reproductive filter selecting for specificity based on mate availability, and co-evolved immunocompatibility where parasites use the same or similar immune-signaling molecules as their hosts to avoid immunological surveillance and response.