Abnormal spermiogenesis is associated with the X-linked sex-ratio trait in Drosophila simulans

The sex-ratio trait, known in several Drosophila species, results from X-linked meiotic drive that affects Y-bearing sperm and causes males to produce female-biased progeny. We describe spermiogenesis in three types of D. simulans males: wild-type, sex-ratio, and males that bear driver X chromosomes but do not express the sex-ratio trait because of autosomal and Y-linked suppression. Sex-ratio males show numerous spermatid nuclei in abnormal positions throughout their cysts, which occurs rarely, if ever, in the two other types. The degree of the spermiogenic failure in sex-ratio males is correlated with the bias towards females in their progeny. This proves that the trait is a case of meiotic drive and strongly suggests that the abnormal spermatids are Y-bearing ones. The number of cysts per testis, hence the production of X-bearing sperm, is not increased in sex-ratio males. Implications for the spread of the sex-ratio trait in natural populations of D. simulans are discussed.