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Sex Change in the Gobiid Fish Is Mediated through Rapid Switching of Gonadotropin Receptors from Ovarian to Testicular Portion or Vice Versa

Laboratory of Reproductive Biology (Y.K., T.U., T.K., B.P.-P., Y.N.), National Institute for Basic Biology, Okazaki 444-8585, Japan; Sesoko Station (Y.K., M.N.), Tropical Biosphere Research Center, University of the Ryukyus, Okinawa 905-0227, Japan; Division of Biological Science (Y.K., N.S.), Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan; Solution Oriented Research for Science and Technology (M.N., T.U., B.P.-P., Y.N.), Japan Science and Technology Corp., Saitama, Japan; Field Science Center (T.S.), Tokyo University of Marine Science and Technology, Tateyama 294-0308, Japan; Laboratory of Molecular Developmental Biology (T.K.), Matsuyama Station, South Ehime Fisheries Research Center, Ehime University, Matsuyama 790-8566, Japan; and General Education Kagoshima University (H.M.), Kagoshima 890-0065, Japan

Address all correspondence and requests for reprints to: Prof. Yoshitaka Nagahama, Laboratory of Reproductive Biology, National Institute for Basic Biology, Okazaki 444-8585, Japan. E-mail: nagahama{at}nibb.ac.jp.

Sex-changing fish Trimma okinawae can change its sex back and forth from male to female and then to male serially, depending on the social status in the harem. T. okinawae is well equipped to respond to its social status by possessing both ovarian and testicular tissues even though only one gonad remains active at one time. Here we investigated the involvement of gonadotropins in sex change by determining the changes in gonadotropin receptor (GtHR) gene expression during the onset of sex change from female to male and male to female. The expression of the GtHR was found to be confined to the active gonad of the corresponding sexual phase. During the sex-change from female to male, initially the ovary had high levels of FSHR and LHR, which eventually went up in the testicular tissue if the fish was bigger. Changing of the gonads started with switching of GtHR expression discernible within 8–12 h of the visual cue. Further in vitro culture of the transitional gonads with a supply of exogenous gonadotropin (human chorionic gonadotropin) revealed that the to-be-active gonad acquired the ability to produce the corresponding sex hormone within 1 d of the activation of GtHR. Conversely, the to-be-regressed gonad did not respond to the exogenous gonadotropin. Our findings show that the gonads of successive sex-changing fish possess the intrinsic mechanism to respond to the social cue differentially. Additionally, this location switching of GtHR expression also could substantiate the importance of the hypothalamo-pituitary-gonadotropic axis.