Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species

Abstract

Genomes are vulnerable to selfish genetic elements that enhance their own transmission often at the expense of host fitness. Examples are cytoplasmic elements such as maternally inherited bacteria that cause feminization, male-killing, parthenogenesis and cytoplasmic incompatibility. We demonstrate, for the first time, that segregation distortion, a phenomenon so far seen only for nuclear genetic elements, can also be caused by a cytoplasmic element, the ubiquitous endosymbiotic bacterium Wolbachia. For Eurema mandarina butterfly lineages with a Z0 sex chromosome constitution, we provide direct and conclusive evidence that Wolbachia induces production of all-female progeny by a dual role: the compensation for the female-determining function that is absent in Z0 lineages (feminization) and the prevention of maternal sex chromosome inheritance to offspring as a specific type of segregation distortion. Therefore, our findings highlight that both sex determination and chromosome inheritance -- crucially important developmental processes of higher eukaryotes -- can be manipulated by cytoplasmic parasites.