Primary males guide the femaleness through the regulation of testicular Dmrt1 and ovarian Cyp19a1a in protandrous black porgy

Controlling the development of the sexes is critically important for the broodstock management in aquaculture. Sex steroids are widely used for sex control of fish. However, hermaphroditic fish have a plastic sex, and a stable sex is difficult to maintain with sex steroids. We used the black porgy (Acanthopagrus schlegelii) as a model to understand the possible mechanism of sexual fate decision. Low exogenous estradiol (E2) induced male development. In contrast, high exogenous E2 induced the regression of the testis and the development of the ovary and resulted in an unstable expression of femaleness (passive femaleness, with ovaries containing only the primary oocytes). The removal of testicular tissue by surgery resulted in the early development of vitellogenic oocytes and active femaleness. Our data also demonstrated that the male-to-female sex change is blocked by the maintenance of male function with gonadotropin-induced dmrt1 expression in the testis. Furthermore, our data also indicated that ovarian cyp19a1a expression is regulated by the testis through epigenetic modifications. Therefore, the primary male guides the femaleness in the protandrous black porgy and the transition of sexual fate from male to female is determined by the status of the testicular tissue.