Divergent allocation of sperm and the seminal proteome along a competition gradient in Drosophila melanogaster

Significance

Ejaculate quality plays an essential role in fertility, sperm competition, and offspring health. A key modulator of ejaculate quality is the social environment. Although males across taxa are known to strategically allocate sperm in response to rivals, how this applies to myriad other ejaculate components is poorly resolved. Here, we take a multilevel approach, from protein to fitness, to show that Drosophila melanogaster males divergently allocate sperm and seminal fluid proteins along a competition gradient. Using a combination of fluorescence-labeled sperm, quantitative proteomics, and multimating assays, we demonstrate that males are remarkably sensitive to the intensity of competition they perceive, show compositional change across and within portions of the ejaculate, and that this compositional change carries distinct costs and benefits.

Abstract

Sperm competition favors large, costly ejaculates, and theory predicts the evolution of allocation strategies that enable males to plastically tailor ejaculate expenditure to sperm competition threat. While greater sperm transfer in response to a perceived increase in the risk of sperm competition is well-supported, we have a poor understanding of whether males ( i) respond to changes in perceived intensity of sperm competition, ( ii) use the same allocation rules for sperm and seminal fluid, and ( iii) experience changes in current and future reproductive performance as a result of ejaculate compositional changes. Combining quantitative proteomics with fluorescent sperm labeling, we show that Drosophila melanogaster males exercise independent control over the transfer of sperm and seminal fluid proteins (SFPs) under different levels of male–male competition. While sperm transfer peaks at low competition, consistent with some theoretical predictions based on sperm competition intensity, the abundance of transferred SFPs generally increases at high competition levels. However, we find that clusters of SFPs vary in the directionality and sensitivity of their response to competition, promoting compositional change in seminal fluid. By tracking the degree of decline in male mating probability and offspring production across successive matings, we provide evidence that ejaculate compositional change represents an adaptive response to current sperm competition, but one that comes at a cost to future mating performance. Our work reveals a previously unknown divergence in ejaculate component allocation rules, exposes downstream costs of elevated ejaculate investment, and ultimately suggests a central role for ejaculate compositional plasticity in sexual selection.