Table_1_Males, the Wrongly Neglected Partners of the Biologically Unprecedented Male–Female Interaction of Schistosomes.xlsx

Schistosomes are the only platyhelminths that have evolved separate sexes, and they exhibit a unique reproductive biology because the female’s sexual maturation depends on a constant pairing contact with the male. In the female, pairing leads to gonad differentiation, which is associated with substantial morphological changes, and controls among others the expression of gonad-associated genes. In the male, no morphological changes have been observed after pairing, although first data indicated an effect of pairing on gene transcription. Comprehensive transcriptomic approaches have revealed an unexpected high number of genes that are differentially transcribed in the male after pairing. Their identities suggest roles for the male that are not restricted to feeding and enhanced muscular power to transport paired female and, as assumed before, to induce its sexual maturation by one “magic” factor. Instead, a more complex picture emerges in which both partners live in a reciprocal sender-recipient relationship that not only affects the gonads of both genders but may also involve tactile stimuli, transforming growth factor β signaling, nutritional parts, and neuronal processes, including neuropeptides and G protein-coupled receptor signaling. This review provides a summary of transcriptomics including an overview of genes expressed in a pairing-dependent manner in schistosome males. This may stimulate further research in understanding the role of the male as the recipient of the female’s signals upon pairing, the male’s “capacitation,” and its subsequent competence as a sender of information. The latter process finally transforms a sexually immature, autonomous female without completely developed gonads into a sexually mature, partially non-autonomous female with fully differentiated gonads and enormous egg production capacity.

吸虫是唯一进化出分离性别的扁形动物，其独特的生殖生物学特征体现在雌性性成熟依赖于与雄性的持续配对接触。在雌性个体中，配对可导致性腺分化，并与显著的形态学变化相关联，进而调控包括性腺相关基因在内的多种基因表达。而在雄性个体中，配对后未观察到形态学变化，尽管初步数据表明配对对基因转录有影响。全面的转录组学方法揭示了在配对后雄性中差异转录的基因数量异常之多。这些基因的功能暗示了雄性在生殖过程中的作用不仅局限于摄食和增强肌肉力量以运输配对的雌性，以及如先前所假设的，通过一种“神秘”因子诱导雌性的性成熟。相反，一个更为复杂的图景浮现，其中双方处于一种相互的发送-接收关系中，这不仅影响两性性腺，还可能涉及触觉刺激、转化生长因子β信号传导、营养分配以及神经元过程，包括神经肽和G蛋白偶联受体信号传导。本综述总结了转录组学，包括对吸虫雄性中依赖配对的基因表达的概述。这或许能激发进一步研究，以理解雄性作为雌性信号接收者的角色，其“激活”状态，以及作为信息发送者的后续能力。最终，这一过程将一个性未成熟、自主性强的雌性个体，其性腺尚未完全发育，转变为一个性成熟、部分非自主的雌性个体，其性腺完全分化，并具有巨大的卵产卵能力。