Research Status and Breeding Application of Sex Reversal in Teleosts Fish
LIU Jia-Nan1,2, WANG Wei2,3, WU Li-Xin1, HU Hong-Xia2,3,*
1 College of Fisheries and Life Sciences, Dalian Ocean University, Dalian 116000, China; 2 Fisheries Research Institute of Beijing Academy of Agriculture, Forestry Sciences/Beijing Key Laboratory of Fishery Biotechnology, Beijing 100068, China; 3 Key Laboratory of Sturgeon Genetics and Breeding, Ministry of Agriculture and Rural Affairs, Hangzhou 311799, China
Abstract:In teleosts fish, some species have significant differences in breeding benefits due to male and female dimorphism. In order to improve the efficiency of aquaculture, monoculture is one of the goals of these fish breeding. Sex reversal, as one of the effective means to achieve unisexual breeding through sex-controlled breeding, has always been a hot topic in teleosts fish reproduction and breeding research. In this paper, the known teleosts fish natural sex reversal phenomenon, sex reversal method, sex reversal mechanism and current application in teleosts fish breeding are described, which provides a theoretical reference for molecular breeding for new varieties of high quality and accelerating the improvement of fish breeding efficiency.
刘佳南, 王巍, 吴立新, 胡红霞. 性逆转在硬骨鱼类中的研究现状及育种应用[J]. 农业生物技术学报, 2025, 33(1): 200-207.
LIU Jia-Nan, WANG Wei, WU Li-Xin, HU Hong-Xia. Research Status and Breeding Application of Sex Reversal in Teleosts Fish. 农业生物技术学报, 2025, 33(1): 200-207.
[1] 戴生飞. 2022. Dmrt1和Foxl3在尼罗罗非鱼性别分化和生殖细胞命运决定中的功能研究[D].博士学位论文, 西南大学, 导师: 王德寿, 李明辉, pp. 5-6. (Dai S F.2022. Functional analysis of Dmrt1 and Foxl3 in sex differentiation and germ cell sexual fate decision of Nile tilapia[D]. Thesis for Ph.D., Southwest University, Supervisor: Wang D S, Li M H, pp. 5-6.) [2] 陈立黎. 2016. 雌、雄激素对罗非鱼性别分化和性腺基因表达的影响[D]. 硕士学位论文, 西南大学, 导师: 王德寿. (Chen L L.2016. The effects of estrogen and androgen on sex differentiation and gonadal gene expression[D]. Thesis for M. S., Southwest University. Supervisor: Wang D S, pp. 1-5.) [3] 陈淑吟, 张志勇, 刘海林, 等. 2017. 池养黑鲷性逆转组织学观察[J]. 海洋科学, 41(7): 51-58. (Chen S Y, Zhang Z Y, Liu H L, et al.2017. Histological observation of sex change in the cultivated black porgy Acanthopagrus schlegeli[J]. Marine Sciences, 41(7): 51-58.) [4] 李加儿, 区又君. 2000. 深圳湾沿岸池养黄鳍鲷的繁殖生物学[J]. 浙江海洋学院学报(自然科学版), (02): 139-143. (Li J E, OU Y J.2000. Studies on the reproductive biology of the pond-cultured Sparus latus houttuyn in the coast of Shenzhen bay[J]. Journal of Zhejiang Ocean University (Natural Science Edition), (02): 139-143.) [5] 李梦茹. 2014. 尼罗罗非鱼两种芳香化酶(Cyp19a1a和Cyp19a1b)表达与功能的初步研究[D]. 博士学位论文, 西南大学, 导师: 王德寿, pp. 1-3. (Li M R.2014. Preliminary studies on expression and function of Cyp19a1a and Cyp19a1b in Nile tilapia[D]. Thesis for Ph. D., Southwest University, Supervisor: Wang D S, pp. 1-3.) [6] 梁冬冬. 2017. 牙鲆性类固醇激素合成重要基因表达调控的初步研究[D]. 硕士学位论文, 中国科学院大学, 中国科学院海洋研究所, 导师: 尤锋, pp. 39-65. (Liang D D.2017. Study on steroidgenesis important genes' expression and regulation in the olive flounder Paralichthys olivaceus[D]. Thesis for M.S., University of Chinese Academy of Sciences, Institute of Oceanology, Chinese Academy of Sciences, Supervisor: You F, pp.39-65.) [7] 欧密, 赵建, 罗青, 等. 2022. 鳢性别控制育种及应用研究进展[J]. 中国农业科技导报, 24(02): 11-25. (Ou M, Zhao J, Luo Q, et al.Research progress on the breeding and application of sex control in snakehead[J]. Journal of Agricultural Science and Technology, 24(02): 11-25.) [8] 齐飘飘, 陈敏, 于跃, 等. 2021. 高温和皮质醇对黄颡鱼性别分化的影响[J]. 水生生物学报, 45(01): 106-117. (Qi P P, Chen M, Yu Y, et al.Effects of high temperature and cortisol on sex differentiation of yellow catfish(Tachysurus Fulvidraco)[J]. Acta Hydrobiologica Sinica, 45(01): 106-117.) [9] 王盈颖. 2015. 赤点石斑鱼和青石斑鱼性分化过程中性腺发育的研究[D]. 硕士学位论文, 厦门大学, 导师: 刘敏, pp. 11-12. (Wang Y Y.2015. Study on gonadal development during sexual differentiation of red-spotted grouper and blue-spotted grouper[D]. Thesis for M. S., Xiamen University, Supervisor: Liu M, pp. 11-12.) [10] 王瑶瑶. 2019. 高温处理的尼罗罗非鱼性腺分化过程及性别决定相关基因时空表达模式研究[D]. 硕士学位论文, 山东农业大学, 导师: 陈红菊, 季相山, pp. 29-30. (Wang Y Y.2019. Gonad development examination and temporal and spatial expression pattern analysis of sex differentiation related genes in high temperature treated female Nile tilapia[D]. Thesis for M.S., Shandong Agricultural University, supervisor: Chen H J, Ji X S, pp. 29-30.) [11] 王浚宇. 2020. 高温和甲基睾酮联合处理对尼罗罗非鱼性别分化的影响研究[D]. 硕士学位论文, 山东农业大学, 导师: 季相山, pp. 30-31. (Wang J Y.2020. Effects of cotreatment with high temperature and methyltestosterone on sex differentiation of Nile tilapia[D]. Thesis for M.S., Shandong Agricultural University, Supervisor: Ji X S, pp. 30-31.) [12] 王德寿, 柳兴永, 李明辉, 等. 2021. 一种高效生产尼罗罗非鱼高繁殖率YY转化雌鱼的方法[P]. 中国,110583539B. (Wang D S, Liu X Y, Li M H, et al.2021. A method for efficient production of Nile tilapia with high reproductive rate YY transformation of female fish[P]. China, 110583539B) [13] 王茂元, 黄洪贵, 钟全福, 等. 2021. 苯甲酸雌二醇对新吉富罗非鱼雌性化的影响[J]. 渔业研究, 43(01): 67-72. (Wang M Y, Huang H G, Zhong Q F, et al.2021. Study on the effect of estradiol benzoate on feminization of the New Gift Tilapia (Oreochromis niloticus)[J]. Journal of Fisheries Research, 43(01): 67-72.) [14] 杨家驹, 黄增岳, 肖耀兴, 等. 1996. 人工诱导巨石斑鱼性逆转的研究[J]. 热带海洋,(04):75-79, 92. (Yang J J, Huang Z Y, Xiao Y X, et al.1996. Artificial induction of sex reversal eversal in the grouper, Epinephelus tauvina (Forskal)[J]. Tropical Oceans,(04): 75-79, 92.). [15] 喻杰, 杨弘. 2020. 鱼类性别决定的遗传基础及性别控制技术在水产养殖中的应用[J]. 大连海洋大学学报, 35(2): 161-168. (Yu J, Yang H.2020. Genetic basis of sex determination and application of sex control in fish: A review[J] Journal of Dalian Fisheries University, 35(2): 161-168.) [16] 赵会宏, 何琪, 张春丽, 等. 2022. 雌雄同体鱼类性别分化及性转变研究进展[J]. 水产学报, 46(04): 644-656. (Zhao H H, He Q, Zhang C L, et al.2022. A review of studies on sex differentiation and sex change in hermaphroditic fishes[J]. Acta Fisheries Sinica, 46(04): 644-656.) [17] 钟汶蓉. 2023. 二倍体泥鳅的雌核发育及性逆转技术研究[D]. 硕士学位论文, 大连海洋大学, 导师: 胡炜, pp. 4-6. (Zhong W R.2023. Induction of meiotic gynogenesis and sex reversal in diploid Misgurnus anguillicaudatus[D]. Thesis for M.S., Dalian Ocean University, Supervisor: Hu W, pp. 4-6.) [18] 邹记兴, 胡超群, 黄增岳, 等. 2000. 外源混合激素诱导巨石斑鱼性逆转的研究[J]. 高技术通讯, (01): 6-10. (Zou J X, Hu C Q, Huang Z Y, et al.2000. Exogenous mixed-hormonal induction of precocious sex reversal in the grouper, Epinephelus tauvina (ForskDl)[J]. High Technology Communications, (01): 6-10.) [19] 邹记兴, 陶友宝, 向文洲, 等. 2003. 人工诱导点带石斑鱼性逆转的组织学证据及其机制探讨[J]. 高技术通讯, (06): 81-86. (Zou J X, Tao Y B, Xiang W Z, et al. 2003. Histological evidence and mechanism in artificial inducement of sex reversal of the grouper, Epinephelus malabaricus[J]. High Technology Communications, (06): 81-86.) [20] Afonso L, Wassermann G, Oliveira R.2001. Sex reversal in Nile tilapia (Oreochromis niloticus) using a nonsteroidal aromatase inhibitor[J] Journa of Experimental Zoology, 290(2): 177-181. [21] Aguilera G, Liu Y.2012. The molecular physiology of CRH neurons[J]. Frontiers in Neuroendocrinology, 33: 1-3. [22] Armstrong B M, Lazorchak J M, Jensen K M, et al.2016. Reproductive effects in fathead minnows (Pimphales promelas) following a 21d exposure to 17α-ethinylestradiol[J]. Chemosphere, 144: 366-373. [23] Avise J C, Mank J E.2009. Evolutionary perspectives on hermaphroditism in fishes[J]. Sexual Development, 3(2-3): 152-163. [24] Baekelandt S, Leroux N, Burattin L, et al.2023. Estetrol has a lower impact than 17α-ethinylestradiol on the reproductive capacity of zebrafish (Danio rerio)[J]. Aquatic Toxicology, 259: e106505. [25] Bhandari R K, Komuro H, Nakamura S, et al.2003. Gonadal restricting and correlative steroid hormone profiles during natural sex change in protogynous honeycomb grouper (Epinephelus merra)[J]. Zoological Society of Japan, (11): 1399-1404. [26] Bjerselius R, Lundstedt-Enkel K, Olsén H, et al.2001. Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17β-estradiol[J]. Aquatic Toxicology, 53(2):139-152. [27] Casas L, Saborido-Rey F, Ryu T, et al.2016. Sex change in clownfish: Molecular insights from transcriptome analysis[J]. Scientific Reports, 6: e35461. [28] Cortés D C C, Padilla L F A, Langlois V S, et al.2019. The central nervous system acts as a transducer of stress-induced masculinization through corticotropin-releasing hormone B[J]. Development, 146: e172866. [29] Chen J, Chen H, Peng C, et al.2019. A highly efficient method of inducing sex change using social control in the protogynous orange-spotted grouper (Epinephelus coioides)[J]. Aquaculture, 517: e734787. [30] Dussenne M, Gennotte V, Rougeot C, et al.2020. Consequences of temperature-induced sex reversal on hormones and brain in Nile tilapia (Oreochromis niloticus)[J]. Hormones and Behavior, 121: e104728. [31] Dries L A.2003. Peering through the looking glass at a sexual parasite: Are amazon mollies red queens?[J]. Evolution, 57(6): 1387-1396. [32] Flynn S R, Benfey T J.2007. Effects of dietary estradiol-17β in juvenile short nose sturgeon, Acipenser brevirostrum, Lesueur[J]. Aquaculture, 270: 405-412. [33] Gao W Q, Bohl Casey E, Dalton James T.2005.Chemistry and structural biology of androgen receptor[J]. Chemical reviews, 105(9): 3352-3370. [34] Gonsioroski A, Mourikes V E, Flaws J A.2020. Endocrine disruptors in water and their effects on the reproductive system[J]. International Journal of Molecular Sciences, 21(6): e1929. [35] Heemers H V, Tindall D J.2007. Androgen receptor (AR) coregulators: A diversity of functions converging on and regulating the AR transcriptional complex[J]. Endocrine Reviews, 28(7): 778-808. [36] Horie Y, Kanazawa N, Takahashi C, et al.2021. Exposure to 4‐nonylphenol induces a shift in the gene expression of gsdf and testis‐ova formation and sex reversal in Japanese medaka (Oryzias latipes)[J]. Journal of Applied Toxicology, 41(3): 399-409. [37] Kitano T, Takamune K, Nagahama Y.et al.2000. Aromatase inhibitor and 17α-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus)[J]. Molecular Reproduction and Development, 56(1): 1-5. [38] Lau E L, Lee M F, Chang C F.2013. Conserved sex-specific timing of meiotic initiation during sex differentiation in the protandrous black porgy Acanthopagrus schlegelii[J]. Biology of Reproduction, 88(150): 1-13. [39] Lin F M, Tong F, He Q, et al.2020. In vitro effects of androgen on testicular development by the AR-foxl3- rec8/fbxo47 axis in orange-spotted grouper (Epinephelus coioides)[J]. General and Comparative Endocrinology, 292: e113435. [40] Lin L L, Janz D M.2006. Effects of binary mixtures of xenoestrogens on gonadal development and reproduction in zebrafish[J] Aquatic Toxicology, 80(4): 382-395. [41] Liu H, Todd E V, Lokman P M.et al.2016. Sexual plasticity: A fishy tale[J]. Molecular Reproduction and Development, 84(2): 171-194. [42] Lyu Q, Hu J, Yang X, et al.2018. Expression profiles of dmrt1 and foxl2 during gonadal development and sex reversal induced by 17α-methyltestosterone in the orange-spotted grouper[J]. General and Comparative Endocrinology, 274: 26-36. [43] Mei J, Gui J F.2015. Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish[J]. Science China (Life Sciences), 58(02): 124-136. [44] Miya M, Gotoh R O, Sado T.2020. MiFish metabarcoding: A high-throughput approach for simultaneous detection of multiple fish species from environmental DNA and other samples[J]. Fisheries Science, 86(6): 939-970. [45] Murata R, Kobayashi Y, Karimata H, et al.2014. Transient sex change in the immature Malabar grouper, Epinephelus malabaricus, androgen treatment[J]. Biology of Reproduction, 91(25): 1-7. [46] Mommsen T, Vijayan M M, Moon T.1999. Cortisol in teleosts: Dynamics, mechanisms of action, and metabolic regulation[J]. Reviews in Fish Biology and Fisheries, 9: 211-268. [47] Navarro-martín L, Viñas J, Ribas L, et al.2011. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass[J]. Public Library of Science (PLoS), (12): e1002447. [48] Örn S, Holbech H, Norrgren L.2016. Sexual disruption in zebrafish (Danio rerio) exposed to mixtures of 17α-ethinylestradiol and 17β-trenbolone[J]. Environmental Toxicology and Pharmacology, 41: 225-231. [49] Piferrer F.2001. Endocrine sex control strategies for the feminization of teleost fish[J]. Aquaculture, 197: 229-281. [50] Rutherford R, Lister A, Bosker T, et al.2020. Mummichog (Fundulus heteroclitus) are less sensitive to 17α-ethinyl estradiol (EE2) than other common model teleosts: A comparative review of reproductive effects[J]. General and Comparative Endocrinology, 289: e113378. [51] Senol G, Kenan G, Osman O.2006. The effect of estradiol valerate on sex reversal of rainbow trout, Oncorhynchus mykiss[J]. Science Alert, (3): 240-243. [52] Shao C W, Li Q Y, Chen S L, et al.2014. Epigenetic modification and inheritance in sexual reversal of fish[J]. Cold Spring Harbor Laboratory, (4): 604-615. [53] Smith I E, Dowsett M.2003. Aromatase inhibitors in breast cancer[J]. New England Journal of Medicine, 348(24): 2431-2442. [54] Todd E V, Liu H, Muncaster S, et al.2016. Bending genders: The biology of natural sex change in fish[J]. Sexual Development, 10(5-6): 223-241. [55] Uchida D, Yamashita M, Kitano T.et al.2004. An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal[J]. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 137(1): 11-20. [56] Vizziano-Cantonnet D, Baron D, Mahè S, et al.2008. Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal trans differentiation[J]. Bioscientifica, (5): 277-288. [57] Wang Q, Liu Y, Peng C, et al.2017. Molecular regulation of sex change induced by methyltestosterone-feeding and methyltestosterone-feeding withdrawal in the protogynous orange spotted grouper[J]. Biology of reproduction, 97(2): 324-333. [58] Wu G C, Tomy S, Lee M F, et al.2010. Sex differentiation and sex change in the protandrous black porgy, Acanthopagrus schlegeli[J]. General and Comparative Endocrinology, 167(3):417-421. [59] Wu G C, Tey W G, Li H W, et al.2015. Sexual fate reprogramming in the steroid-induced bi-directional sex change in the protogynous orange-spotted grouper, Epinephelus coioides[J]. PLOS ONE, 10(12): e0145438. [60] Yamaguchi T, Yoshinaga N, Yazawa T, et al.2010. Cortisol is involved in temperature-dependent sex determination in the Japanese flounder[J] The Endocrine Society, (8): 3900-3908. [61] Yang Y, Liu Q H, Xiao Y S, et al.2018. High temperature increases the gsdf expression in masculinization of genetically female Japanese flounder (Paralichthys olivaceus)[J]. General and Comparative Endocrinology, 274: 17-25. [62] Yeh S L, Kuo C M, Ting Y Y, et al.2003. Androgens stimulate sex change in protogynous grouper, Epinephelus coioides: Spawning performance in sex-changed males[J]. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 135(3): 375-382. [63] Yuan H W, Chen F, Xu Q Q, et al.2011. Effects of exogenous melatonin on serum steroid hormones, GSI, survival ratio and sex reversal in rice field eel, (Monopterus albus)[J]. Applied Mechanics and Materials, (142): 238-242. [64] Zohar Y, Abraham M, Gordin H.1978. The gonadal cycle of the captivity-reared hermaphroditic teleost Sparus aurata (L.) during the first two years of life[J]. Annales de Biologie Animale, Biochimie, Biophysique, (18): 877-882. [65] Zhao Y, Chen J H, Wang Y Y, et al.2020. Gonad development examination of high-temperature-treated genetically female Nile tilapia[J]. Aquaculture, 515: e7.