Genetic Signature of Reproductive Manipulation in the Phylogeography of the Bat Fly, Trichobius major

Abstract

The bat fly (Trichobius major) is a blood-feeding ectoparasite of the cave myotis (Myotis velifer). A recent mitochondrial DNA (mtDNA) study examining population structure of T. major in the South Central United States detected a single haplotype from all individuals examined (N = 48 from 12 different caves), representing one of only a few known examples of such widespread mtDNA uniformity. We examined nuclear genetic diversity using amplified fragment length polymorphism and detected high levels of nuclear genetic diversity in all populations sampled. Amplified fragment length polymorphism analyses indicated significant levels of gene flow among caves >700 km apart, suggesting the absence of mtDNA diversity in T. major is the result of a selective sweep, not a demographic event (i.e., a recent bottleneck). One mechanism by which mtDNA sweeps occur in arthropods is through bacterial parasites that manipulate host reproduction and mtDNA inheritance. We used PCR to test for the presence of all known reproductive parasites and detected a widespread infection (91.33% infection rate) of T. major with a novel Arsenophonus bacterium, as well as the infection of 2 individuals (1.16% infection rate) with a novel strain of Rickettsia. We discuss the implications for T. major phylogeography and the necessity of a bigenomic approach in arthropod population genetics.

Evolution, Multiple Acquisition, and Localization of Endosymbionts in Bat Flies (Diptera: Hippoboscoidea: Streblidae and Nycteribiidae)

“…Trowbridge et al (6) documented an Arsenophonus-like bacteria in several fly species belonging to the genus Trichobius (Streblidae, Trichobiinae). This was subsequently corroborated by Lack et al (10) for several populations of Trichobius major and by Nováková et al (11) for an unknown Trichobius species. Arsenophonus spp.…”

“…Because of limited sampling throughout the known geographic ranges of Basilia and Nycteribia, whether this is truly a replacement rather than a transient infection remains ambiguous, and the frequency of such replacements remains unclear. Streblid endosymbionts identified by Trowbridge et al (6), Lack et al (10), and Nováková et al (11) were previously assigned to the genus Arsenophonus. In our analysis, they form their own, novel monophyletic lineage (clade B), which is distinct from but allied to "Candidatus Riesia pediculicola" (Fig.…”

“…are widespread Gammaproteobacteria that show a great diversity of symbiotic relationships with their arthropod hosts, ranging from reproductive parasites, facultative symbionts of unknown function, to vertically transmitted obligate mutualists (7,(11)(12)(13)(14)(15)(16)(17)(18)(19). In addition to mutualistic roles, Lack et al (10) hypothesized that Arsenophonus manipulates host reproduction in T. major.…”

Some Like It Hot: Evolution and Ecology of Novel Endosymbionts in Bat Flies of Cave-Roosting Bats (Hippoboscoidea, Nycterophiliinae)

“…They belong to the Hippoboscoidea, a group that also encompasses tsetse flies (Glossinidae, see above) and louse flies (Hippoboscidae). Previous studies have identified bacterial symbionts associated with the nycteribiid genera Basilia, Nycteribia, Penicillidia, and Phthiridium (21,28), and the streblid genus Trichobius (31,56). Some of these symbionts are vertically transmitted, and sequences seem to form a monophyletic clade associated with the presumed mutualist bacteria found in sucking lice ("Candidatus Riesia") (37).…”

“…(i) What is the relationship of bacterial associates in Nycterophiliinae to known bacterial associates in other insects and bat flies? Based on prior evidence from bat flies, it can be expected that Nycterophiliinae harbor bacterial symbionts and that these are likely related to symbionts within the Gammaproteobacteria (21,31,56).…”