Males, the Wrongly Neglected Partners of the Biologically Unprecedented Male–Female Interaction of Schistosomes

Abstract

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.

Dynamic Expression of Long Non-Coding RNAs Throughout Parasite Sexual and Neural Maturation in Schistosoma Japonicum

“…Gene ontology enrichment analysis showed that hundreds of protein-coding genes related to neuron projection, differentiation, nervous system development, and G-protein receptor signaling pathways were present in the brown module ( Figure 7 and Supplementary File 4). This confirms that, both in S. mansoni and S. japonicum, sexually mature males have a more active neuronal regulation than sexually mature females, including those mediated by G-protein signaling, which might point to a higher importance of neuronal processes in males during reproduction [21]. We found that some module eigengenes had opposite patterns of change as a function of the days post-infection in males and females, such as in the brown module (Figure 6d).…”

Identificação e anotação de RNAs longos não-codificantes em Schistosoma mansoni e Schistosoma japonicum

“…7 and Supplementary Data 4). This confirms that, both in S. mansoni and S. japonicum, sexually mature males have a more active neuronal regulation than sexually mature females, including those mediated by G-protein signaling, which may point to a higher importance of neuronal processes in males during reproduction [21].…”

Schistosome japonicum Proteins that Interact with the Gynecophoral Canal Protein Identified Using a Yeast Two-hybrid System

“…The stimuli from the male worms play important roles in the growth and reproductive development of female worms [6], and these stimuli are independent of sperm transfer and fertilization [4,[7][8][9]. The male worms are proposed to deliver speci c molecules to female worms during pairing; the molecules associated this "magic male factor" have been unveiled in studies of the gynecophoral canal protein (GCP) [10].…”

“…Studies of S. japonicum have revealed that GCP is necessary for pairing to occur between male and female worms [24]. Although the biochemical activity of GCP has not yet been clearly de ned, there is accumulating evidence for its participation in male-female interaction in these worms [10].…”