Oocytes Survive in the Testis by Altering the Soma Fate from Male to Female in the Protandrous Black Porgy, Acanthopagrus schlegeli1

Abstract

In fish, hermaphroditism is derived from gonochorism. No ancient ancestry and no single sex-determining mechanism are involved in the hermaphroditic fish. Furthermore, hermaphroditic fish have a common set of transcriptional regulators that are involved in gonadal differentiation. However, the origins and evolution of hermaphroditism in fish remain far from understood. In the protandrous black porgy (Acanthopagrus schlegeli Bleeker), the ovotestis is separated by connective tissue, and no intersex (ectopic germ cell) characteristics are observed in either part. We generated the abnormal testicular part of the ovotestis with estradiol-17beta (E2) treatment, in which newly regenerated testis has ectopic oocytes. In this study, we performed a detailed phenotypic and molecular analysis of these E2-induced ectopic oocytes in the testicular part of the ovotestis. We showed that the oocytes in the regenerated testis do not undergo apoptosis; thus, a number of oocytes are in the testis. In these oocytes, Figla has a prolonged expression with ectopic expression of Cyp19a1a. Strikingly, the cells surrounding the oocytes are Dmrt1-positive cells (putative Sertoli cells) with high Figla expression in the oocytes at an early stage. Then, as the Dmrt1 expression diminishes, Cyp19a1a-positive cells (putative follicle cells) with low Figla expression appear in the oocytes at a later stage. This finding indicates that oocytes are competent to create a microenvironment to protect against a testicular environment in black porgy fish. Furthermore, Figla likely is the key factor in the pathway of Sertoli cell transformation into follicle-like cells. These results shed light on why the presence of more than one sex at a time existed during an evolutionary transition from gonochorism to hermaphroditism in fish.