D. melanogaster meiotic driver Stellate compromises sperm development by impeding nuclear envelope remodeling

Meiotic drive is a phenomenon that violates Mendel’s Law of Equal Segregation, leading to biased transmission of the meiotic driver to the offspring. D. melanogaster Stellate (Ste) is an X-linked meiotic driver that preferentially harms Y-chromosome-bearing spermatids, thereby favoring the transmission of the X chromosome to the next generation. We have recently shown that Ste protein segregates asymmetrically during meiosis I with a strong bias toward the Y-chromosome-inheriting side, leading to the eventual demise of the Y-chromosome-containing spermatids. However, the cellular mechanisms by which Ste protein interferes with spermatid development remain unknown. Here, we show that Ste-containing spermatids are delayed in the process of nuclear envelope remodeling, an essential process during sperm DNA compaction. We show that Lamin Dm0, a component of the nuclear lamina, is rapidly removed during nuclear envelope remodeling during the early stages of normal spermatid development. However, Ste-containing spermatid retained Lamin Dm0 for a prolonged time. Delayed Lamin Dm0 removal is associated with defective formation of the dense complex, which is composed of the bundle of microtubules and serves as a structural support for sperm nuclear morphogenesis. Defective dense complex formation in Ste-containing spermatid led to defective sperm DNA compaction. Together, the present study reveals an unexpected cellular mechanism by which a meiotic driver, Ste, sabotages sperm development.