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 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 expressed during post-meiotic stages of spermatogenesis, when spermatid elongation occurs, and we found that it is rapidly evolving under positive selection in Drosophila. Hypomorphic knockout of Eip74EF leads to shorter sperm but does not affect SR length, suggesting that Eip74EF may be involved in promoting spermatid elongation but is not a genetic driver of male-female coevolution. We also found that Eip74EF knockout 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 knockout males produce more sperm that are also shorter, which would explain the increase in fecundity, but this hypothesis remains to be tested. Our results suggest a novel function of Eip74EF in spermatogenesis and demonstrates that this gene influences both male and female reproductive success.