Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the germline at the expense of the soma, suggesting differential impacts of aging on sperm and seminal fluid and trade-offs between them or, more broadly, between reproduction and lifespan. While harmful effects of male age on sperm are well known, we do not know how much seminal fluid deteriorates in comparison. Moreover, given the predicted trade-offs, it remains unclear whether systemic lifespan-extending interventions could ameliorate the declining performance of the ejaculate as a whole. Here, we address these problems using Drosophila melanogaster. We demonstrate that seminal fluid deterioration contributes to male reproductive decline via mating-dependent mechanisms that include posttranslational modifications to seminal proteins and altered seminal proteome composition and transfer. Additionally, we find that sperm production declines chronologically with age, invariant to mating activity such that older multiply mated males become infertile principally via reduced sperm transfer and viability. Our data, therefore, support the idea that both germline and soma components of the ejaculate contribute to male reproductive aging but reveal a mismatch in their aging patterns. Our data do not generally support the idea that the germline is prioritized over soma, at least, within the ejaculate. Moreover, we find that lifespan-extending systemic down-regulation of insulin signaling results in improved late-life ejaculate performance, indicating simultaneous amelioration of both somatic and reproductive aging.

随着男性年龄的增长，射精能力下降在分类学上很普遍，并且具有广泛的健康影响。射精成功需要功能齐全的种系（精子）和体细胞（精液）成分。然而，一些衰老理论预测，资源应该以牺牲体细胞为代价优先转移到种系，这表明衰老对精子和精液的不同影响以及它们之间的权衡，或者更广泛地说，生殖和寿命之间的权衡。虽然男性年龄对精子的有害影响众所周知，但我们不知道相比之下，精液会恶化多少。此外，考虑到预期的权衡，目前尚不清楚系统性的延长寿命的干预措施是否可以改善整体射精性能下降的情况。在这里，我们使用果蝇解决这些问题。我们证明，精液恶化通过交配依赖性机制导致男性生殖能力下降，其中包括精液蛋白的翻译后修饰以及精液蛋白质组组成和转移的改变。此外，我们发现精子产量随着年龄的增长而下降，这与交配活动无关，因此老年多次交配的雄性主要通过精子转移和活力的减少而变得不育。因此，我们的数据支持这样的观点，即射精的种系和体细胞成分都有助于男性生殖衰老，但揭示了它们的衰老模式不匹配。我们的数据通常不支持生殖系优先于体细胞的观点，至少在射精中是这样。此外，我们发现，延长寿命的胰岛素信号系统性下调会改善晚年射精性能，表明躯体衰老和生殖衰老同时得到改善。