Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster

In the Drosophila lineage, both sperm and the primary female sperm storage organ, the seminal receptacle (SR), may reach extraordinary lengths. In D. melanogaster, long SRs bias fertilization toward long sperm during the displacement stage of sperm competition. This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. To further understand the costs and benefits of long sperm and SR genotypes in both sexes, we measured male and female fitness in inbred lines of D. melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs, or short SRs. We specifically asked: do long SRs impose costs or benefits on the females that bear them? Do genotypes that generate long sperm in males impose a fitness cost on females sharing those genotypes? Is long sperm an honest indicator of male viability and associated with increased fitness? And finally, are the benefits of long sperm restricted to competitive fertilization success, or do long-sperm males also have increased mating success and fecundity in single matings? We found that both sexes have increased longevity in long sperm and long SR genotypes, with fewer reproduction-related benefits and evidence for trade-offs in males, compared to females. Our results suggest that sperm length and SR length are both indicators of increased viability.