Drosophila seminal sex peptide associates with rival as well as own sperm, providing SP function in polyandrous females.

ABSTRACT

When females mate with more than one male, the males' paternity share is affected by biases in sperm use. These competitive interactions occur while female and male molecules and cells work interdependently to optimize fertility, including modifying the female's physiology through interactions with male seminal fluid proteins (SFPs). Some modifications persist, indirectly benefiting later males. Indeed, rival males tailor their ejaculates accordingly. Here, we show that SFPs from one male can directly benefit a rival's sperm. We report that Sex Peptide (SP) that a female Drosophila receives from a male can bind sperm that she had stored from a previous male, and rescue the sperm utilization and fertility defects of an SP-deficient first-male. Other seminal proteins received in the first mating 'primed' the sperm (or the female) for this binding. Thus, SP from one male can directly benefit another, making SP a key molecule in inter-ejaculate interaction.

When fruit flies and other animals reproduce, a compatible male and a female mate, allowing sperm from the male to swim to and fuse with the female's egg cells. The males also produce proteins known as seminal proteins that travel with the sperm. These proteins increase the likelihood of sperm meeting an egg and induce changes in the female that increase the number, or quality, of offspring produced. Some seminal proteins help a male to compete against its rivals by decreasing their chances to fertilize eggs. However, since many of the changes seminal proteins induce in females are long-lasting, it is possible that a subsequent male may actually benefit indirectly from the effects of a prior male's seminal proteins. It remains unclear whether the seminal proteins of one male are also able to directly interact with and help the sperm of another male. Male fruit flies make a seminal protein known as sex peptide. Normally, a sex peptide binds to the sperm it accompanies into the female, increasing the female's fertility and preventing her from mating again with a different male. To test whether the sex peptide from one male can bind to and help a rival male's sperm, Misra and Wolfner mated female fruit flies with different combinations of males that did, or did not, produce the sex peptide. The experiments found that female flies that only mated with mutant males lacking the sex peptide produced fewer offspring than if they had mated with a 'normal' male. However, in females that mated with a mutant male followed by another male who provided the sex peptide, the second male's sex peptide was able to bind to the mutant male's sperm (as well as to his own). This in turn allowed the mutant male's sperm to be efficiently used to sire offspring, at levels comparable to a normal male providing the sex peptide. These findings demonstrate that the ways individual male fruit flies interact during reproduction are more complex than just simple rivalry. Since humans and other animals also produce seminal proteins comparable to those of fruit flies, this work may aid future advances in human fertility treatments and strategies to control the fertility of livestock and pests, including mosquitoes that transmit diseases.