Rapid Genomic Adaptation of Drosophila Melanogaster to Wolbachia Elimination

Symbionts can confer multifaceted fitness advantages to their hosts, thereby shaping host gene evolution. Wolbachia, the most prevalent intracellular bacteria in insects, modulates numerous host physiological traits and can induce cytoplasmic incompatibility between infected and uninfected individuals. While artificial trans-infection of Wolbachia into different hosts has been extensively studied, the adaptive evolution of naturally infected hosts after Wolbachia removal remains unclear. In this study, we treated Wolbachia-infected Drosophila melanogaster lineage with tetracycline to generate an uninfected line, maintaining the original infected line as the control. Both populations were subsequently reared under identical conditions for 69 generations. Two populations exhibited significant genomic divergence and mating discrimination, replicate parallel populations showed highly consistent differentiation patterns. Transposable elements and other non-coding genes underwent strong positive selection, and male-biased genes experienced heightened selective pressure. We further demonstrated that immune genes play a crucial role in Drosophila adaptation to Wolbachia loss, with immune traits exhibiting sex-specific evolutionary trajectories. Allelic differentiation at the odorant-binding protein genes Obp19b and Obp19c may underlie hybrid barriers between the two populations. Our results dissect how symbiont precipitates rapid, sex-specific genomic and behavioural change, providing a tractable model for symbiont-driven population divergence. Removal of Wolbachia can rapidly influence host genomic divergence and sex-biased gene expression differentiation. Using experimental evolution, we reveal rapid, sex-specific divergence driven by immune genes and odorant-binding proteins. These findings uncover symbiont-driven population divergence mechanisms.