BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

Abstract

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1,000 fertility-enhancing “main cells” and ∼40 more functionally cryptic “secondary cells.” Inhibition of bone morphogenetic protein (BMP) signaling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female postmating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary-cell secretions might therefore make highly specific contributions to the seminal proteome and ejaculate function; alternatively, they might regulate more global—but hitherto undiscovered—SFP functions and proteome composition. Here, we present data that support the latter model. We show that in addition to previously reported phenotypes, secondary-cell-specific BMP signaling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main-cell–derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell types, suggesting that modification to the cellular make-up of seminal-fluid-producing tissues is an important factor in ejaculate evolution.

TheDrosophilaseminal proteome and its role in postcopulatory sexual selection

“…Neuronal pathways that control sperm ejection [120] or other aspects of sperm use, storage and retention [51] might represent targets for interference by Sfps to promote success of that male's sperm. Consistent with this idea, males whose secondary cell function has been manipulated transfer an altered seminal proteome, and when these males are the first of two males, their mates are slower to eject the sperm of second males [81].…”

“…In this case, females mated to these genetically manipulated males appear to release fewer sperm per fertilized egg, again resulting in the over-retention of sperm [81]. However, mates of these males remate much more quickly [30,81], meaning that the net effect of the royalsocietypublishing.org/journal/rstb Phil. Trans.…”

Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila

“…Having identified loss of ejaculate performance associated with increased age and mating activity, and the direct contribution of the seminal fluid, we next investigated whether changes to the seminal fluid proteome could explain these effects. We applied label-free quantitative proteome analysis to the Sfp-producing tissues (accessory glands and ejaculatory duct) of experimental males ( 31 – 33 ).…”

Seminal fluid and accessory male investment in sperm competition

“…[121]), because of the relatively simple genetic basis of the underlying traits. Extracting functionally relevant axes of genetic variation or their underlying gene regulatory networks [104,[122][123][124] will further help to reduce dimensionality and define the most evolutionarily relevant seminal fluid variation.…”