Gonadal Restructuring and Correlative Steroid Hormone Profiles during Natural Sex Change in Protogynous Honeycomb Grouper (Epinephelus merra)

Abstract

The honeycomb grouper shows protogynous hermaphroditism. The endocrine mechanisms involved in gonadal restructuring throughout protogynous sex change are largely unknown. In the present study, we investigated changes in the gonadal structures and levels of serum sex steroid hormones during female to male sex change in the honeycomb grouper. On the basis of histological changes, entire process of sex change was assigned into four developmental phases: female, early transition (ET), late transition (LT), and male phase. At the female phase, the oocytes of several developmental stages were observed including gonial germ cells in the periphery of ovigerous lamellae. At the beginning of ET phase, perinucleolar and previtellogenic oocytes began degenerating, followed by proliferation of spermatogonia toward the center of lamella. The LT phase was characterized by further degeneration of oocytes and rapid proliferation of spermatogenic germ cells throughout the gonad. At the male phase, no ovarian cells were observed and testis had germ cells undergoing active spermatogenesis. Serum levels of estradiol-17beta (E2) were high in females in the breeding season, but low in the non-breeding female, transitional and male phase, and those of 11-ketotestosterone (11-KT) and testosterone (T) were low in females and gradually increased in the transitional and male phase. The present results suggest that low serum E2 levels and degeneration of oocytes accompanied by concomitant increase in the 11-KT levels and proliferation of spermatogenic germ cells are probably the events mediating protogynous sex change in the honeycomb grouper.

Anti‐Müllerian hormone and 11 β‐hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males

“…The roles of 11-KT were investigated in protogynous hermaphrodite fish species that showed similar gonadal morphology during the natural sex reversal process to that observed in juvenile zebrafish (Wang et al, 2007). Increased 11-KT concentrations were observed during the natural ovarytestis transition in several species, such as Thalassoma dupperrey (Nakamura et al, 1989), Sparisoma viride (Cardwell and Liley, 1991), and Epinephelus merra (Bhandari et al, 2003;Alam et al, 2006). Artificial female-tomale sex reversal could also be induced by treating individuals of two of these species with 11-KT (Cardwell and Liley, 1991;Bhandari et al, 2006).…”

Molecular mechanisms underlying sex change in hermaphroditic groupers

“…Previous studies have focused mainly on the descriptions of gonad ultrastructure and histology at different developmental stages (Smith 1965;Moe 1969;Tan and Tan 1974;Bruslé and Bruslé 1975;Kuo et al 1988;Bruslé-Sicard et al 1992;Johnson et al 1998;Marino et al 2001;Bhandari et al 2003). Marino et al (2001) have depicted gonad morphology of the dusky grouper (E. marginatus) by the histological observation of 405 individuals from the Pelagie Islands in the Mediterranean Sea.…”

“…In males, 11-KT, teleost-specific androgen, is considered a principal androgen in teleostean fish, and it plays a central role in sexual maturation, development of secondary sexual characteristics and reproductive behaviour (Miura et al 1991;Borg 1994). In many sexchanging fish, the levels of circulating 11-KT have been reported to increase with the progression of sex change (Nakamura et al 1989;Johnson et al 1998;Kroon and Liley 2000;Bhandari et al 2003), and exogenous 11-KT treatment can induce sex reversal (Kroon and Liley 2000;Yeh et al 2003). It was found that the androgen-producing sites exist in the ovary of honeycomb grouper (Alam et al 2005) and that naturally occurring sex change is accompanied by significant increases in the size of androgen-producing cells and production of androgen by the gonads .…”

“…In the honeycomb grouper, female-to-male sex change was shown to be associated with a drop in E2 levels followed by an increase in androgen levels. Thus, Bhandari et al (2003) suggested that a drop in E2 levels alone might be the key to the onset of sex change in the honeycomb grouper, and that increased T and 11-KT levels following gonadal transformation could be stimulatory to male germ-cell proliferation and differentiation in the ovary. For many fishes, an endogenous estrogen-androgen balance maintains sexual phenotypes.…”

“…For example, the honeycomb grouper, E. merra, is one of smallest species in the genus Epinephelus, in which the mean total length (TL) of females does not exceed 20 cm. In other words, 20 cm in TL is a threshold size for sex change (Bhandari et al 2003). In the dusky grouper (E. marginatus), the sexual maturity is first reached when females are 5 years old and 40-50 cm in total length, while sex change occurs when individuals are 9 to 16 years old and 70-90 cm in total length (Chauvet 1988).…”