Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera).

Queens of many social hymenoptera keep sperm alive within their specialized storage organ, the spermatheca, for years, defying the typical trade-off between lifespan and reproduction. However, whether honey bee (Apis mellifera) queens experience a trade-off between reproduction and immunity is unknown, and the biochemical processes underlying sperm viability are poorly understood. Here, we survey quality metrics and viral loads of honey bee queens from nine genetic sources. Queens rated as ‘failed’ by beekeepers had lower sperm viability, fewer sperm, and higher levels of sacbrood virus and black queen cell virus. Quantitative proteomics on N = 123 spermathecal fluid samples shows, after accounting for sperm count, health status, and apiary effects, five spermathecal fluid proteins significantly correlating with sperm viability: odorant binding protein (OBP)14, lysozyme, serpin 88Ea, artichoke, and heat-shock protein (HSP)10. The significant negative correlation of lysozyme—a conserved immune effector—with sperm viability is consistent with a reproduction vs. immunity trade-off in honey bee queens. Honey bee queens store and use sperm for years after mating, but doing so may require a dampened immune response to keep the sperm viable. Alison McAfee et al. tested this hypothesis using mass spectrometry-based proteomics in queens with high and low sperm quantity and quality and found that lower measures of fertility correlated with high levels of the immune effector lysozyme, consistent with a trade-off between immunity and fertility.