Mammalian sperm must spend a minimum period of time within a female reproductive tract to achieve the capacity to fertilize oocytes. This phenomenon, termed sperm ‘capacitation’, was discovered nearly seven decades ago and opened a window into the complexities of sperm–female interaction. Capacitation is most commonly used to refer to a specific combination of processes that are believed to be widespread in mammals and includes modifications to the sperm plasma membrane, elevation of intracellular cyclic AMP levels, induction of protein tyrosine phosphorylation, increased intracellular Ca2+ levels, hyperactivation of motility, and, eventually, the acrosome reaction. Capacitation is only one example of post‐ejaculatory modifications to sperm (PEMS) that are widespread throughout the animal kingdom. Although PEMS are less well studied in non‐mammalian taxa, they likely represent the rule rather than the exception in species with internal fertilization. These PEMS are diverse in form and collectively represent the outcome of selection fashioning complex maturational trajectories of sperm that include multiple, sequential phenotypes that are specialized for stage‐specific functionality within the female. In many cases, PEMS are critical for sperm to migrate successfully through the female reproductive tract, survive a protracted period of storage, reach the site of fertilization and/or achieve the capacity to fertilize eggs. We predict that PEMS will exhibit widespread phenotypic plasticity mediated by sperm–female interactions. The successful execution of PEMS thus has important implications for variation in fitness and the operation of post‐copulatory sexual selection. Furthermore, it may provide a widespread mechanism of reproductive isolation and the maintenance of species boundaries. Despite their possible ubiquity and importance, the investigation of PEMS has been largely descriptive, lacking any phylogenetic consideration with regard to divergence, and there have been no theoretical or empirical investigations of their evolutionary significance. Here, we (i) clarify PEMS‐related nomenclature; (ii) address the evolutionary origin, maintenance and divergence in PEMS in the context of the protracted life history of sperm and the complex, selective environment of the female reproductive tract; (iii) describe taxonomically widespread types of PEMS: sperm activation, chemotaxis and the dissociation of sperm conjugates; (iv) review the occurence of PEMS throughout the animal kingdom; (v) consider alternative hypotheses for the adaptive value of PEMS; (vi) speculate on the evolutionary implications of PEMS for genomic architecture, sexual selection, and reproductive isolation; and (vii) suggest fruitful directions for future functional and evolutionary analyses of PEMS.

中文翻译：

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射精后精子修饰（PEMS）


哺乳动物精子必须在雌性生殖道内停留最短时间才能达到使卵母细胞受精的能力。这种被称为精子“获能”的现象在近七十年前被发现，为了解精子与女性相互作用的复杂性打开了一扇窗。获能最常用于指被认为广泛存在于哺乳动物中的特定过程组合，包括精子质膜的修饰、细胞内环磷酸腺苷水平的升高、蛋白质酪氨酸磷酸化的诱导、细胞内Ca2+水平的增加、细胞内Ca2+的过度激活。运动，以及最终的顶体反应。获能只是射精后精子修饰（PEMS）的一个例子，这种修饰在动物界广泛存在。尽管 PEMS 在非哺乳动物类群中的研究较少，但它们可能代表了体内受精物种的规则而不是例外。这些 PEMS 形式多样，共同代表了精子复杂成熟轨迹选择的结果，其中包括专门针对女性阶段特定功能的多种连续表型。在许多情况下，PEMS 对于精子成功迁移通过女性生殖道、在长时间的储存中存活、到达受精部位和/或实现使卵子受精的能力至关重要。我们预测 PEMS 将表现出由精子与雌性相互作用介导的广泛表型可塑性。因此，PEMS 的成功执行对于适应性的变化和交配后性选择的运作具有重要意义。 此外，它可能提供一种广泛的生殖隔离和物种边界维持机制。尽管它们可能普遍存在并且很重要，但 PEMS 的研究很大程度上是描述性的，缺乏任何关于分歧的系统发育考虑，并且没有对其进化意义进行理论或实证研究。在这里，我们 (i) 澄清 PEMS 相关术语； (ii) 在精子漫长的生命史和女性生殖道复杂的选择性环境的背景下解决 PEMS 的进化起源、维持和分歧； (iii) 描述在分类学上广泛存在的 PEMS 类型：精子激活、趋化性和精子结合物的解离； (iv) 审查 PEMS 在整个动物界的发生情况； (v) 考虑 PEMS 适应性价值的替代假设； (vi) 推测 PEMS 对基因组结构、性选择和生殖隔离的进化影响； (vii) 为 PEMS 未来的功能和进化分析提出富有成果的方向。