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

Abstract

Meiotic drive is a phenomenon that violates Mendels 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 components of the nuclear lamina (such as Lamin Dm0, and the LEM domain proteins Otefin and Bocks) are rapidly removed during nuclear envelope remodeling during the early stages of normal spermatid development. However, Ste-containing spermatids retained these nuclear lamina proteins for a prolonged time. Their delayed removal is associated with defective formation of the dense complex, which is composed of a bundle of microtubules and serves as a structural support for sperm nuclear morphogenesis. Defective dense complex formation in Ste-containing spermatids led to defective sperm DNA compaction. Together, the present study reveals an unexpected cellular mechanism by which a meiotic driver, Ste, sabotages sperm development. Article summaryStellate is an X-chromosome-linked meiotic driver in D. melanogaster, which interferes with the process of spermatogenesis and causes preferential death of the Y-chromosome-containing spermatids. However, the cellular mechanisms by which Stellate interferes with spermatogenesis remain unknown. This study shows that Stellate-containing spermatids are defective in the process of nuclear envelope remodeling, an essential process during sperm DNA compaction. Defective nuclear envelope remodeling was associated with a failure to assemble the dense complex, a microtubule-rich structure that serves as structural support for sperm nuclear morphogenesis. Together, the study provides insights into a cellular strategy employed by a meiotic driver.