The effects of prostomium and proventriculus removal on sex determination and gametogenesis inTyposyllis pulchra (Polychaeta: Syllidae)

Abstract

The prostomium alone or the prostomium and proventriculus of reproductiveTyposyllis pulchra were periodically removed at known stages of oogenesis and the gametes were examined by transmission electron microscopy. If the proventriculus and prostomium were simultaneously removed prior to day 3 of the stolonization sequence, before gonial differentiation, the time reruired for stolon formation and concomitant gametogenesis was shortened; the animals, all of which had previously reproduced as females, produced only ultrastructurally normal sperm. Spermatogenesis in these induced males began earlier in the stolonization period than in normal males. However, the cytological events of spermatogenesis were not accelerated. When the same operation was performed after differentiated oocytes were present, gamete cytodifferentiation and development time did not appear to be affected and the animals remained female. Removal of the prostomium alone, formerly thought to have no effect, caused high mortality and if removed prior to day 3 appeared to prevent both stolonization and gametogenesis. Ultrastructural investigation of these animals shows that gonads are maintained, but that gonial cells fail to differentiate or produce gametes. The subsequent removal of the proventriculus and regenerating prostomium from these animals allows them to mature as induced males. This suggests a prostomial role in regulating the endocrine activity of the proventriculus during the reproductive cycle.

Regeneration mechanisms in Syllidae (Annelida)

“…Following studies were focused mainly on the relationship between regeneration and sexual reproduction based on experiments of removal of the pharynx and/or proventricle, which might play a role during stolonization (Durchon, , ; Junqua, ; Okada, ; Wissocq, , ). Some of the most recent studies were those published by Franke (, ), Heacox and Schroeder (), and Franke and Pfannenstiel (). After three decades, this topic re‐emerged with a study about the role of the proventricle during the stolonization of T. antoni (Weidhase, Bleidorn et al., ).…”

“…Usually, experiments with removal of the proventricle indicated a potential role of this structure during reproduction (Durchon, , ; Franke, , ; Franke & Pfannenstiel, ; Weidhase, Beckers et al., ). Posterior ends of fragments without proventricle seem to increase the production of male stolons, suggesting that the proventricle inhibits the stolonization and is involved in sexual determination (Durchon, , ; Durchon & Wissocq, ; Franke & Pfannenstiel, ; Heacox & Schroeder, ; Weidhase, Beckers et al., ; Wissocq, ). Experiments in which the proventricle is removed in S. prolifera have shown that stolonization stops when the structure is re‐implanted, indicating that the proventricle may inhibit stolonization while promoting regeneration (Franke & Pfannenstiel, ).…”

“…Most studies dealing with regeneration in syllids were published at the end of the 19th century (Langerhans, 1879;Malaquin, 1893;Marion & Bobretzky, 1875) and during the 20th century (Allen, 1923;Boilly & Thibaut, 1974;Delye, 1962;Durchon, 1959;Franke, 1980;Heacox & Schroeder, 1982;Junqua, 1957;Michel, 1909b;Okada, 1929;Wissocq, 1966). The first experiment under laboratory conditions was conducted with the species Syllis gracilis by Mesnil (1901).…”

Expression of vasa, piwi, and nanos during gametogenesis in Typosyllis antoni (Annelida, Syllidae)

“…Interestingly, syllids are known to have an hormonal regulatory system of sex determination which involves the prostomium and the proventricle (Durchon, 1972;Franke, 1983Franke, , 1986bPfannenstiel, 1978;Weidhase et al, 2016;Wissocq & Wolff, 1966). Moreover, they can present successive (Durchon, 1951;Franke, 1986a;Wissocq, 1963) or even simultaneous hermaphroditism (Musco et al, 2010), and it has been shown that proventricle removal induces the formation of male stolons, indicating that additional mechanisms are necessary for female specification (Durchon, 1951;Heacox & Schroeder, 1982;Weidhase et al, 2016). Therefore, the differences between males and females in the expression patterns of Ta-nanos ( Figure 4) and Ta-vasa ( Figure 6) could also be related to the hormonal regulation of sex determination.…”

Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction in Annelida

“…specialized structure of the digestive tract), allowing the initiation of stolonization (Franke 1999). In contrast, during winter, when days are short and temperatures low at high latitudes, the proventricle is not controlled by the prostomium, and the proventricular stolonization-suppressing hormone then inhibits stolonization (e.g., Abeloos 1950;Durchon 1952Durchon , 1959Durchon and Wissocq 1964;Franke 1980Franke , 1981Franke , 1983aFranke , b, 1985Franke , 1999Heacox 1980;Heacox and Schroeder 1982;Franke and Pfannenstiel 1984;Verger-Bocquet 1984). Hormonal factors have also been suggested to drive the sexual differentiation of the stolon (Franke 1980;Heacox and Schroeder 1982), in particular the female stolon, given that it seems that male stolon differentiation occurs autonomously, whereas female stolon differentiation may depend on hormone release by male stolons (Franke 1999).…”