During speciation, sex chromosomes accumulate interspecific genetic incompatibilities faster than the rest of the genome. As a consequence, X-linked hybrid sterility is often an early stage in the evolution of reproductive isolation. To understand why the X chromosome is a hotspot for the accumulation of hybrid sterility, we have undertaken genetic and population genomic analysis of X-linked hybrid male sterility between two fruit fly sister species, Drosophila mauritiana and D. simulans. We have identified multiple X-linked regions that are sufficient to cause male sterility when introgressed from D. mauritiana into a D. simulans genome. Spermatogenesis in sterile genotypes proceeds through meiosis but does not complete spermatid individualization. Most X-linked sterility results from incompatibly interactions with autosomal alleles, but both genetic and cytological results indicate that one factor causes sterility through interactions with the heterospecific Y chromosome. Previous theory suggests that X-linked sterilizing incompatibilities may arise through the evolution of sex chromosome meiotic drive elements. We find evidence that both supports and rejects this theory, as a known X-linked drive element recently migrated between these species and caused a strong reduction in local sequence divergence. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

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