Abstract
Queens of Acromyrmex leaf-cutting ants store sperm of multiple males after a single mating flight, and never remate even though they may live for decades and lay tens of thousands of eggs. Sperm of different males are initially transferred to the bursa copulatrix and compete for access to the long-term storage organ of queens, but the factors determining storage success or failure have never been studied. We used in vitro experiments to show that reproductive tract secretions of Acromyrmex echinatior queens increase sperm swimming performance by at least 50% without discriminating between sperm of brothers and unrelated males. Indiscriminate female-induced sperm chemokinesis makes the likelihood of storage directly dependent on initial sperm viability and thus provides a simple mechanism to secure maximal possible reproductive success of queens, provided that initial sperm motility is an accurate predictor of viability during later egg fertilization.
Highlights
Sperm compete for direct egg fertilization or access to storage sites, whereas females may bias the outcome by chemically modulating the direction or speed of sperm motility [1,2]
All measurements of sperm motility within the same counting chamber were highly repeatable, which confirmed that our methods were reliable
Sperm velocity (PC1; figure 1c) increased by ca 50% in queen fluids compared with the Hayes controls (F1,104 1⁄4 49.09, p, 0.0001), similar to the three original variables that loaded PC1 (49.4% for VCL, 52.2% for velocity on the average path (VAP), 57.2% for VSL) and once more without segregation between related and unrelated female fluids (F1,104 1⁄4 0.10, p 1⁄4 0.75)
Summary
Sperm compete for direct egg fertilization or access to storage sites, whereas females may bias the outcome by chemically modulating the direction (chemotaxis) or speed (chemokinesis) of sperm motility [1,2]. Exclusive single queen mating is ancestral in all ants, bees and wasps that evolved morphologically distinct queen and worker castes [8,9], but polyandry (the storage of multiple ejaculates) evolved in several evolutionarily derived lineages [10]. In such clades, ejaculates compete for access to the queen’s sperm storage organ (the spermatheca), from where sperm will be used to fertilize eggs for up to several decades [11]. This should imply strong selection for storing only viable sperm until the maximal storage capacity is reached
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