A novel role for Eip74EF in male reproduction in promoting sperm elongation at the cost of fecundity

Spermatozoa are the most morphologically variable cell type, yet little is known about genes controlling natural variation in sperm shape. Drosophila fruit flies have evolved the longest sperm known, which are evolving under postcopulatory sexual selection, driven by sperm competition and cryptic female choice. Long sperm outcompete short sperm but primarily when females have long seminal receptacles (SRs), the primary sperm storage organ. Thus, selection on sperm length is mediated by SR length, and the two traits are coevolving across the Drosophila lineage, driven by a genetic correlation and fitness advantage of long sperm and long SR genotypes in both males and females. Ecdysone induced protein 74EF (Eip74EF) is rapidly evolving under positive selection in Drosophila, and it is expressed during post-meiotic stages of spermatogenesis, when spermatid elongation occurs. Partial knockdown of Eip74EF leads to shorter sperm but does not affect SR length, suggesting that Eip74EF is involved in promoting spermatid elongation but is not a genetic driver of male-female coevolution. We also found that Eip74EF knockdown has opposing effects on fecundity in males and females, with an increase in fecundity for males but a decrease in females, consistent with its documented role in oocyte maturation. It is possible that knockdown males produce more sperm that are also shorter, which would explain the increase in fecundity, but this hypothesis remains to be tested. Our results document a novel function of Eip74EF in spermatogenesis and demonstrates that this gene influences both male and female reproductive success.

精子是形态多样性最高的细胞类型，但目前学界对调控精子形态自然变异的基因仍知之甚少。果蝇（Drosophila）演化出了已知最长的精子，这类精子在交配后性选择的作用下持续演化，该选择由精子竞争与隐蔽雌性选择驱动。长精子相较于短精子更具竞争优势，但该优势仅在雌性拥有较长的储精囊（seminal receptacle, SR）——这是主要的精子储存器官——时才会显现。因此，精子长度所受的选择压力由储精囊长度介导，这两个性状在果蝇演化支系中呈现协同演化关系，其驱动因素为雌雄个体中长精子与长储精囊基因型所具备的遗传相关性与适合度优势。蜕皮激素诱导蛋白74EF（Ecdysone induced protein 74EF, Eip74EF）在果蝇中处于正向选择下的快速演化状态，其在精子发生的减数后阶段（即精子细胞伸长阶段）得以表达。对Eip74EF的部分敲低会导致精子长度缩短，但不会影响储精囊长度，这表明Eip74EF参与促进精子细胞伸长，但并非雌雄协同演化的遗传驱动因子。本研究还发现，Eip74EF敲低对雌雄个体的繁殖力具有相反作用：雄性繁殖力提升，而雌性繁殖力下降，这与其在卵母细胞成熟中已被报道的功能相一致。敲低后的雄性可能产生更多且更短的精子，这或许可以解释其繁殖力提升的现象，但该假说仍有待验证。本研究结果揭示了Eip74EF在精子发生中的全新功能，并证实该基因同时影响雌雄个体的繁殖成功率。