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In internally fertilizing species, sperm transfer is not always immediately followed by egg fertilization, and female sperm storage (FSS) may occur. FSS is a phenomenon in which females store sperm in a specialized organ for periods lasting from a few hours to several years, depending on the species. Eusocial hymenopterans (ants, social bees, and social wasps) hold the record for FSS duration. In these species, mating takes place during a single nuptial flight that occurs early in adult life for both sexes; they never mate again. Males die quickly after copulation but survive posthumously as sperm stored in their mates' spermathecae. Reproductive females, also known as queens, have a much longer life expectancy, up to 20 years in some species. Here, we review what is currently known about the molecular adaptations underlying the remarkable FSS capacities in eusocial hymenopterans. Because sperm quality is crucial to the reproductive success of both sexes, we also discuss the mechanisms involved in sperm storage and preservation in the male seminal vesicles prior to ejaculation. Finally, we propose future research directions that should broaden our understanding of this unique biological phenomenon.

Sperm cells age during storage in the male reproductive organs, which can lead ejaculate quality to decline dramatically over time. Such may pose a particular concern in species with constrained sperm supplies, where adult males cannot replenish their sperm reserves. In eusocial hymenopterans (i.e. ants, bees and wasps with permanent castes), males typically reach adulthood with a limited quantity of sperm, and their testes deteriorate shortly thereafter. In adult life, both sexes mate during a single reproductive event. While males die quickly after copulation, they persist posthumously via sperm stored in their mates' spermatheca, sometimes for decades. As a result of this mating system, males should experience intense selection pressure to produce and transfer high‐quality sperm. Using the black garden ant (Lasius niger) as a model system, we investigated whether the duration of storage in the accessory testes before copulation affected sperm quality. We found that there was no impact of male age on sperm number or viability and that sperm DNA fragmentation decreased rather that increased with age. These results highlight the extent to which male ants, and possibly other taxa with constrained sperm supplies, have evolved extremely specialized strategies to ensure reproductive performance.

Sperm competition is a pervasive evolutionary force that shapes sperm traits to maximize fertilization success. Indeed, it has been shown to increase sperm production in both vertebrates and invertebrates. However, sperm production is energetically costly, which may result in trade-offs among sperm traits. In eusocial hymenopterans, such as ants, mating dynamics impose unique selective pressures on ejaculate. Males are sperm limited: they enter adulthood with a fixed amount of sperm that will not be renewed. We explored whether sperm competition intensity was associated with sperm quantity and quality (i.e. sperm viability and DNA fragmentation) in nine Cataglyphis desert ants. Our results provide phylogenetically robust evidence that sperm competition is positively correlated with sperm production and sperm viability. However, it was unrelated to sperm DNA integrity, indicating the absence of a trade-off involving this trait. These findings underscore that sperm competition may strongly mould sperm traits and drive reproductive performance in eusocial Hymenoptera.

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