Sperm length and seminal fluid proteins promote male reproductive success in <i>Drosophila melanogaster</i>

Spermatozoal morphology varies widely within and among species, often corresponding to the shape of the female sperm storage organs in ways that can impact fertilization. To understand genetic mechanisms of sperm length variation, we compared gene expression patterns in the testes of Drosophila melanogaster males that produce either long or short sperm. We found that genes upregulated in long sperm testes are enriched for long noncoding RNAs and seminal fluid proteins (Sfps). Transferred to the female during mating, Sfps are secreted by the male accessory glands and affect female remating rate, physiology, and behavior. While sperm and Sfps are both critical for male reproductive success, they are largely considered to be functionally and genetically independent, and Sfps have no known function in testes. Knockouts of two Sfps upregulated in long sperm males, Sex Peptide and ovulin, resulted in shorter sperm, suggesting Sfps may contribute to sperm length development. Consistent with this, knockout of accessory gland function did not affect sperm length, indicating accessory gland expression had no influence on spermatogenesis. We also found that long sperm males were better able to delay female remating, suggesting a dual advantage in sperm competition by both delaying female remating and resisting sperm displacement. However, we found that the delay in female remating does not necessarily increase progeny or paternity success. Thus, multiple components of the ejaculate promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain.