The phage gene wmk is a candidate for male killing by a bacterial endosymbiont

Abstract

Wolbachia are the most widespread maternally-transmitted bacteria in the animal kingdom. Their global spread in arthropods and varied impacts on animal physiology, evolution, and vector control are in part due to parasitic drive systems that enhance the fitness of infected females, the transmitting sex of Wolbachia. Male killing is one common drive mechanism wherein the sons of infected females are selectively killed. Despite decades of research, the gene(s) underlying Wolbachia-induced male killing remain unknown. Here using comparative genomic, transgenic, and cytological approaches in fruit flies, we identify a candidate gene in the eukaryotic association module of Wolbachia prophage WO, termed WO-mediated killing (wmk), which transgenically causes male-specific lethality during early embryogenesis and cytological defects typical of the pathology of male killing. The discovery of wmk establishes new hypotheses for the potential role of phage genes in sex-specific lethality, including the control of arthropod pests and vectors. Male killing is an adaptive trait for bacteria that are maternally transmitted through host populations. Such bacteria are common in arthropods and resultantly have significant impacts on host population size, mating strategy, and evolution. Moreover, male-killing bacteria are under recent scrutiny as a symbiotic strategy for arthropod pest and vector control. Despite decades of research, the microbial genetic basis of Wolbachia-induced male killing remains elusive. Here we demonstrate that a single gene from the eukaryotic association module in prophage WO of Wolbachia is a candidate for male killing as it recapitulates many aspects of the phenotype when transgenically expressed in fruit flies. This discovery represents a step forward in understanding new roles of phage WO genes in shaping arthropod hosts and may inform the potential use of male killing in worldwide pest and vector control strategies.