Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation?

The evolution of sperm quality and quantity is shaped by various selective processes, with sperm competition generally considered the primary selective agent. Particularly in external fertilizers, however, sperm limitation through gamete dispersal can also influence gamete investments, but empirical data examining this effect are limited. Here, we studied the relative importance of sperm competition and the spawning conditions in explaining the macroevolutionary patterns of sperm size and number within two taxa with external fertilization but differences in their reproductive biology. In frogs, sperm swim slowly but for up to hours as they penetrate the gelatinous egg coating, whereas fish sperm typically swim fast, are very short-lived (seconds to minutes), and often face a relatively higher risk of being moved away from the ova by currents. Our phylogenetic models and path analyses revealed different trajectories of ejaculate evolution in these two taxa. Sperm size and number responded primarily to variation in sperm competition in the anurans, but more strongly to egg number and water turbulence in the fishes. Whereas the results across anurans align with the general expectation that sexual selection is the main driver of ejaculate evolution, our findings across the fishes suggest that sperm limitation has been underappreciated.精子质量与数量的演化受多种选择过程的塑造，其中精子竞争通常被视为核心选择因子。不过，尤其在体外受精生物中，由配子扩散引发的精子限制效应同样会影响配子投入，但验证该效应的实证数据相对匮乏。本研究聚焦两类具备体外受精特征但生殖生物学存在显著差异的类群，探讨精子竞争与产卵环境对精子大小、数量宏观演化模式的相对重要性。在蛙类中，精子游动速度较慢，但可维持长达数小时的活力以穿透胶状卵膜；而鱼类精子通常游动迅捷、寿命极短（仅数秒至数分钟），且往往面临更高的被水流冲离卵子的风险。我们通过系统发育模型与路径分析发现，这两类类群的精液演化轨迹存在显著分异。无尾目（Anura）类群的精子大小与数量主要受精子竞争强度变化的调控，而鱼类的精子特征则更多受到卵子数量与水流扰动的影响。尽管无尾类的研究结果符合“性选择是精液演化主要驱动因素”的主流学术预期，但我们针对鱼类的研究结果表明，精子限制效应长期以来被学界低估。