D3459: Evolution of mutualism from parasitism in a Wolbachia-Drosophila symbiosis

Animal-microbe symbioses are ubiquitous in nature, spanning diverse interactions from facultative parasitism to obligate mutualism. Further, many of these relationships are not strictly parasitic or mutualistic. Indeed, many facultative symbionts co-evolve with their hosts and develop obligate relationships. However, the transition between symbiotic states is rarely observed and little is known about the genetics and mechanisms underlying symbiotic transition points. Here, we report the discovery of a male-killing symbiont that has developed mutualistic traits. Male killing, or selective death of male offspring, is a phenotype that can result when certain strains of Wolbachia bacteria infect their arthropod hosts. We discovered a lineage of Drosophila bifasciata that exhibits developmental and fitness defects when its male-killing Wolbachia symbiont, wBif, is cured via heat or antibiotic treatment. In contrast, a fly lineage that has never carried the symbiont exhibits no defects. These differences are uncharacteristic of hosts infected with male-killing Wolbachia, and it is previously unobserved even in other wBif-D. bifasciata lineages. These results suggest that this is a recent and evolving mutualism where the infected fly lineage has acquired a developmental defect that rescued by wBif. In addition, the mitochondria of the infected lineage are highly divergent from other D. bifasciata lines, and evidence suggests they may be the source of the host developmental defect. This Wolbachia-Drosophila symbiosis represents a new case of a symbiosis in transition to mutualism, and allows rare insight into the molecular changes underlying this phenomenon.