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

Alison Mcafee,Leonard J Foster,Jeffery S Pettis,Abigail Chapman,David R Tarpy

doi:10.1038/s42003-020-01586-w

Abstract

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.

Highlights

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
Long-term sperm storage is a remarkable feature of social insect biology, with hymenopteran queens storing sperm for by far the longest duration of any animal[1]
Much work has been dedicated to sexual selection among males via sperm competition[2,3,4,5,6] and the trade-offs of male and female innate immunity with sperm quality and stored sperm viability[7,8,9,10,11,12]

Summary

Introduction

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. In males of a variety of species, including insects, there is a well-established negative relationship between sperm viability and immune function[8,10,12,17,18,19,20,21] These trade-offs between reproduction and immunity are thought to be driven either by resource-allocation compromises[23,24] or collateral damage of immune effectors[9,10]. The spermatheca is a largely anoxic environment[26], and mated queens upregulate enzymes that combat oxidative stress, like catalase and superoxide dismutase[27,28,29] Both the collateral damage hypothesis and the resource allocation hypothesis predict that immunosuppressed individuals will have higher sperm viability, and likewise, that immune stimulation decreases sperm viability. Mating reduces phenoloxidase activity (an immune effector responsible for the melanization cascade) in wood ant and leaf-cutter ant queens[22,30]

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Results