Department of Biology, Center for Reproductive Evolution, Syacuse University, Syracuse, NY, 13244, USA.
Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY, 14853, USA.
Biol Rev Camb Philos Soc. 2020 Apr;95(2):365-392. doi: 10.1111/brv.12569. Epub 2019 Nov 18.
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 Ca 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.
哺乳动物精子必须在雌性生殖道内停留一段时间，才能具备受精卵子的能力。这种现象被称为精子“获能”，它是近 70 年前发现的，为研究精子与雌性的相互作用打开了一扇窗。获能通常是指一系列被认为在哺乳动物中广泛存在的特定过程的组合，包括对精子质膜的修饰、细胞内环腺苷酸水平的升高、蛋白质酪氨酸磷酸化的诱导、细胞内 Ca 水平的增加、运动的超激活，以及最终的顶体反应。获能只是精子在射精后的修饰（PEMS）的一个例子，这种修饰在动物王国中广泛存在。虽然在非哺乳动物类群中对 PEMS 的研究较少，但它们很可能是内部受精物种的普遍现象，而不是例外。这些 PEMS 在形式上是多种多样的，它们共同代表了选择塑造精子复杂成熟轨迹的结果，这些轨迹包括多个、连续的表型，这些表型专门针对雌性体内的特定功能阶段。在许多情况下，PEMS 对于精子成功通过雌性生殖道迁移、在长时间的储存中存活、到达受精部位和/或具备受精卵子的能力是至关重要的。我们预测，PEMS 将表现出广泛的表型可塑性，这种可塑性是由精子与雌性的相互作用介导的。因此，PEMS 的成功执行对适应度的变化和交配后性选择的运作具有重要意义。此外，它可能提供了一种广泛的生殖隔离机制，并维持了物种边界。尽管它们可能无处不在且非常重要，但对 PEMS 的研究主要是描述性的，缺乏任何关于进化分歧的系统发育考虑，也没有对其进化意义进行理论或实证研究。在这里，我们：（i）澄清了与 PEMS 相关的命名法；（ii）在精子的延长生命史和雌性生殖道的复杂选择环境的背景下，讨论了 PEMS 的进化起源、维持和分歧；（iii）描述了在分类学上广泛存在的 PEMS 类型：精子激活、趋化性和精子结合体的解离；（iv）综述了 PEMS 在整个动物界的发生情况；（v）考虑了 PEMS 适应性价值的替代假说；（vi）推测了 PEMS 对基因组结构、性选择和生殖隔离的进化意义；（vii）提出了未来对 PEMS 进行功能和进化分析的有成效的方向。
