Abstract Production of female gametes is costly; however, there is now wide evidence across different taxa that male ejaculates are also limiting. Thus, multiply mated males may need to partition their ejaculate across successive matings. While more attention has been payed to whether female mating with previously mated males could be sperm limited, there have been fewer studies on depletion of other substances transferred in the male ejaculate such as accessory gland products. Here, we assessed whether male mating frequency affected mating success, copula duration, mating latency, and sperm stored by females. In addition, we measured male testes and accessory gland size across consecutive matings and evaluated the effect of male multiple mating on female fecundity, fertility, and remating propensity in the South American fruit fly, Anastrepha fraterculus . We show that males have the capacity to modulate ejaculate expenditure, and although sperm storage dramatically decreased after the first mating, this had no effect on female reproductive parameters. However, males mating with five consecutive females had smaller accessory glands. Females mated with males who had previously mated five times failed to lay any eggs. This lower propensity to lay eggs could suggest that males become depleted of products synthetized in the accessory glands, including peptides that have an effect on oogenesis and/or egg laying. We discuss our results in terms of cost of production of male accessory gland products and the impact on female fitness according to male mating history. Significance statement During insect copulation, males transfer to females’ seminal fluids composed of sperm and accessory gland (AG) products. Sperm depletion over male consecutive matings and its impact on female reproductive success have been explored in the past years; however, AG depletion and its effects on female physiology and behavior remain practically unexplored. We show for the fruit fly, Anastrepha fraterculus , that male multiple matings have a dramatic impact on female fecundity and fertility after males achieve five copulations, and this effect seems mediated by depletion and lack of replenishment of products synthetized in the AG, inferred through their size reduction. In contrast, while sperm transfer was markedly higher for virgin than for multiply mated males, this did not affect female fecundity or fertility, showing that the dynamics of seminal fluid components can differ.

中文翻译：

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实蝇中雄性附属腺耗竭影响雌性生殖能力，与精子耗竭无关

摘要 雌配子的生产成本高；然而，现在不同分类群的广泛证据表明雄性射精也受到限制。因此，多次交配的雄性可能需要在连续交配中分配他们的射精。虽然更多关注女性与先前交配的男性交配是否会限制精子，但关于消耗男性射精中转移的其他物质（如附属腺体产品）的研究较少。在这里，我们评估了雄性交配频率是否影响交配成功、交配持续时间、交配潜伏期和雌性储存的精子。此外，我们测量了连续交配的雄性睾丸和附属腺体大小，并评估了雄性多次交配对南美果蝇雌性繁殖力、生育力和再交配倾向的影响，按实实蝇。我们表明雄性具有调节射精支出的能力，尽管在第一次交配后精子储存量急剧减少，但这对雌性生殖参数没有影响。然而，与连续五只雌性交配的雄性具有较小的附属腺体。与先前交配过五次的雄性交配的雌性未能产卵。这种较低的产卵倾向可能表明雄性会耗尽辅助腺中合成的产物，包括对卵子发生和/或产卵有影响的肽。我们从男性附属腺产品的生产成本和根据男性交配历史对女性健康的影响来讨论我们的结果。意义说明 在昆虫交配期间，雄性转移到由精子和附属腺 (AG) 产物组成的雌性精液中。过去几年已经探索了雄性连续交配导致的精子消耗及其对雌性生殖成功的影响；然而，AG 耗竭及其对女性生理和行为的影响实际上仍未得到探索。我们为果蝇 Anastrepha fraterculus 证明，在雄性实现五次交配后，雄性多次交配对雌性的繁殖力和生育能力产生了巨大的影响，这种影响似乎是由 AG 中合成的产品的消耗和缺乏补充所介导的，通过它们的推断尺寸减小。相比之下，虽然处女的精子转移率明显高于多次交配的雄性，但这并不影响雌性的繁殖力或生育能力，这表明精液成分的动态可能不同。