Living with a Male-Killer

Bacterial symbionts are universal entities of living organisms that affect host fitness in many ways ranging from facultative parasitism to obligate mutualism in short- but also long-term evolutionary associations. As endosymbionts live inside the host in a complex ecosystem by competing and cooperating with other bacteria and their respective selfish mobile genetic elements (MGEs) like bacteriophages, plasmids and transposons, it is essential for their successful long-term maintenance to coevolve and reach an equilibrium between symbiont- directed costs and benefits. We hypothesise that disruptions of the homeostasis between the host and its reproductive endosymbionts - either by internal or external factors - can trigger changes in their genomic compositions and frequencies towards novel fitness optima of this symbiosis that consequently can reduce even gene flow between subpopulations and thereby drive host speciation. We also propose that the symbionts MGEs the symbionts of the symbiont are important key actors in this process that can drive host fitness indirectly by conflict and cooperation. To study the contribution of symbionts on host fitness we need to better understand the temporal and spatial dynamics of all symbiotic key players in a natural host system that allows us to monitor incipient speciation in motion, like the neotropical Drosophila system uncovered and intensively studied by Dobzhansky since the mid of the 20 th century. As we found in our recent collections from nature, this system is coevolving with two key model endosymbionts and their variants, i.e., Wolbachia and Spiroplasma, both in facultative and obligate associations with neotropical flies. Both microbes are strictly maternally transmitted with high fidelity, maintained in neotropical hosts over long evolutionary distances, enriched with MGEs and can express either mutualistic protective or reproductive parasitic phenotypes like cytoplasmic incompatibilities (CI) or male-killing (MK). We further uncovered in our recent collections, besides rare pathogenic MK Spiroplasma at high densities, another distantly- related but hidden, so-called systemic infection type that is fixed and asymptomatic under normal conditions but turns pathogenic as their native neotropical hosts have developed under higher temperatures. This means that neotropical fly populations exist and evolve in multi- partner symbioses with both pathogenic and systemic Spiroplasma as well as with facultative and obligate Wolbachia endosymbionts in different combinations. This system is unique and perfectly suited for studying the complex functional and evolutionary interplay between microbes and associated MGEs in the model system Drosophila under field and lab conditions by NGS, genetics, cell biology and experimental evolution. Primary researchers involved: Michael GERTH, Univ. Halle, D, and Wolfgang MILLER, Med. Univ. Vienna, A.