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Microbial endosymbiosis is widespread in animals, with major ecological and evolutionary implications. Successful symbiosis relies on efficient vertical transmission through host generations. However, when symbionts negatively affect host fitness, hosts are expected to evolve suppression of symbiont effects or transmission. Here, we show that sex chromosomes control vertical transmission of feminizing  Wolbachia  endosymbionts in the isopod  Armadillidium nasatum . Theory predicts that the invasion of an XY/XX species by cytoplasmic sex ratio distorters is unlikely because it leads to fixation of the unusual (and often lethal or infertile) YY genotype. We demonstrate that  A .  nasatum  X and Y sex chromosomes are genetically highly similar and that YY individuals are viable and fertile, thereby enabling  Wolbachia  spread in this XY-XX species. Nevertheless, we show that  Wolbachia  cannot drive fixation of YY individuals, because infected YY females do not transmit  Wolbachia  to their offspring, unlike XX and XY females. The genetic basis fits the model of a Y-linked recessive allele (associated with an X-linked dominant allele), in which the homozygous state suppresses  Wolbachia  transmission. Moreover, production of all-male progenies by infected YY females restores a balanced sex ratio at the host population level. This suggests that blocking of  Wolbachia  transmission by YY females may have evolved to suppress feminization, thereby offering a whole new perspective on the evolutionary interplay between microbial symbionts and host sex chromosomes.

Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod