Skip to main content
Log in

Studies on feminization, sex determination, and differentiation of the Southern catfish, Silurus meridionalis—a review

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The sex ratio of the feral Southern catfish was reported to be about 1:1, while the fish obtained by artificial fertilization were always female. Hence, we examined the possible influence of the micro-environment during artificial insemination (pH of the ovarian fluid and concentration of the semen) and early development (feed, hatching temperature, and water) on the sex ratio of Southern catfish fry. In order to examine the possibility of the occurrence of gynogenesis during artificial propagation, cytological observations on the insemination processes and the artificial induction of gynogenesis were also performed. However, no male fish were obtained even in these experiments, excluding the possibilities of these micro-environmental changes on catfish sex ratio and the occurrence of gynogenesis during artificial propagation. Female-to-male sex reversal was achieved by treatment with fadrozole (an aromatase inhibitor) and tamoxifen (an estrogen receptor antagonist). Histological analyses on the gonadal development of both female and induced male fish were subsequently performed. Moreover, several genes involved in sex differentiation, such as dmrt1, foxl2, and cyp19, and three subunits of gonadotropin (gth), i.e., gthα, lhβ, and fshβ, were isolated. Their expression patterns were studied under normal gonadal development and sex reversal conditions. The results revealed that dmrt1, foxl2, and cyp19a were closely related to catfish sex differentiation, and the gth subunits were possibly related to ovarian differentiation and oocyte development. Taken together, we hypothesized that estrogen was highly responsible for the ovarian differentiation and feminization of catfish fry under artificial propagation, although the mechanism involved remains elusive.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Afonso LO, Iwama GK, Smith J, Donaldson EM (1999) Effects of the aromatase inhibitor fadrozole on plasma sex steroid secretion and ovulation rate in female coho salmon, Oncorhynchus kisutch, close to final maturation. Gen Comp Endocrinol 113:221–229. doi:10.1006/gcen.1998.7198

    Article  PubMed  CAS  Google Scholar 

  • Baroiller JF, D’Cotta H (2001) Environment and sex determination in farmed fish. Comp Biochem Physiol C Toxicol Pharmacol 130(4):399–409. doi:10.1016/S1532-0456(01)00267-8

    Article  PubMed  CAS  Google Scholar 

  • Baroiller JF, Guiguen Y (2001) Endocrine and environmental aspects of sex differentiation in gonochoristic fish. EXS 91:177–201

    PubMed  CAS  Google Scholar 

  • Baron D, Cocquet J, Xia X, Fellous M, Guiguen Y, Veitia RA (2004) An evolutionary and functional analysis of FoxL2 in rainbow trout gonad differentiation. J Mol Endocrinol 33(3):705–715. doi:10.1677/jme.1.01566

    Article  PubMed  CAS  Google Scholar 

  • Baron D, Houlgatte R, Fostier A, Guiguen Y (2005) Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 73(5):959–966. doi:10.1095/biolreprod.105.041830

    Article  PubMed  CAS  Google Scholar 

  • Baron D, Montfort J, Houlgatte R, Fostier A, Guiguen Y (2007) Androgen-induced masculinization in rainbow trout results in a marked dysregulation of early gonadal gene expression profiles. BMC Genomics 8:357. doi:10.1186/1471-2164-8-357

    Article  PubMed  CAS  Google Scholar 

  • Bhandari RK, Komuro H, Higa M, Nakamura M (2004) Sex inversion of sexually immature honeycomb grouper (Epinephelus merra) by aromatase inhibitor. Zool Sci 21(3):305–310. doi:10.2108/zsj.21.305

    Article  PubMed  CAS  Google Scholar 

  • Bhandari RK, Nakamura M, Kobayashi T, Nagahama Y (2006) Suppression of steroidogenic enzyme expression during androgen-induced sex reversal in Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 145(1):20–24. doi:10.1016/j.ygcen.2005.06.014

    Article  PubMed  CAS  Google Scholar 

  • Bobe J, Montfort J, Nguyen T, Fostier A (2006) Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod Biol Endocrinol 4:39–54. doi:10.1186/1477-7827-4-39

    Article  PubMed  CAS  Google Scholar 

  • Chang XT, Kobayashi T, Kajiura H, Nakamura M, Nagahama Y (1997) Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): changes in P450arom mRNA, protein and enzyme activity in ovarian follicles during oogenesis. J Mol Endocrinol 18:57–66. doi:10.1677/jme.0.0180057

    Article  PubMed  CAS  Google Scholar 

  • Chang XT, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y (2005) Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen Comp Endocrinol 141:101–115. doi:10.1016/j.ygcen.2004.11.020

    Article  PubMed  CAS  Google Scholar 

  • Conover DO, Fleisher MH (1986) Temperature sensitive period of sex determination in the Atlantic silverside, Menidia menidia. Can J Fish Aquat Sci 43:514–520. doi:10.1139/f86-061

    Article  Google Scholar 

  • Craig JK, Foote CJ, Wood CC (1996) Evidence for temperature dependent sex determination in sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 53:141–147. doi:10.1139/cjfas-53-1-141

    Article  Google Scholar 

  • Davis KB, Simco BA, Goudie CA, Parker NC, Cauldwell W, Snellgrove R (1990) Hormonal sex manipulation and evidence for female homogamety in channel catfish. Gen Comp Endocrinol 78(2):218–223. doi:10.1016/0016-6480(90)90008-A

    Article  PubMed  CAS  Google Scholar 

  • D’Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller JF (2001) Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia, Oreochromis niloticus. Mol Reprod Dev 59(3):265–276. doi:10.1002/mrd.1031

    Article  PubMed  Google Scholar 

  • Elbrecht A, Smith RG (1992) Aromatase enzyme activity and sex determination in chickens. Science 255:467–470. doi:10.1126/science.1734525

    Article  PubMed  CAS  Google Scholar 

  • Guan G, Kobayashi T, Nagahama Y (2000) Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the Tilapia (Oreochromis niloticus). Biochem Biophys Res Commun 272(3):662–666. doi:10.1006/bbrc.2000.2840

    Article  PubMed  CAS  Google Scholar 

  • Hudson QJ, Smith CA, Sinclair AH (2005) Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Dev Dyn 233:1052–1055. doi:10.1002/dvdy.20388

    Article  PubMed  CAS  Google Scholar 

  • Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78(2):333–341. doi:10.1095/biolreprod.107.064246

    Article  PubMed  CAS  Google Scholar 

  • Iwamatsu T, Kobayashi H, Sagegami R, Shuo T (2006) Testosterone content of developing eggs and sex reversal in the medaka (Oryzias latipes). Gen Comp Endocrinol 145(1):67–74. doi:10.1016/j.ygcen.2005.07.003

    Article  PubMed  CAS  Google Scholar 

  • Jiao BW (2003) Effects of sex steroids on the sex differentiation of the Southern catfish, Silurus meridionalis Chen. Dissertation, Southwest Normal University of China

  • Kitano T, Takamune K, Kobayashi T, Nagahama Y, Abe SI (1999) Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J Mol Endocrinol 23(2):167–176. doi:10.1677/jme.0.0230167

    Article  PubMed  CAS  Google Scholar 

  • Kitano T, Takamune K, Nagahama Y, Abe SI (2000) Aromatase inhibitor and 17alpha-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol Reprod Dev 56:1–5. doi:10.1002/(SICI)1098-2795(200005)56:1<1::AID-MRD1>3.0.CO;2-3

    Article  PubMed  CAS  Google Scholar 

  • Kitano T, Yoshinaga N, Shiraishi E, Koyanagi T, Abe S (2007) Tamoxifen induces masculinization of genetic females and regulates P450 aromatase and Müllerian inhibiting substance mRNA expression in Japanese flounder (Paralichthys olivaceus). Mol Reprod Dev 74(9):1171–1177. doi:10.1002/mrd.20603

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi T, Kajiura-Kobayashi H, Nagahama Y (2003) Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101:289–294. doi:10.1159/000074351

    Article  PubMed  CAS  Google Scholar 

  • Komatsu T, Nakamura S, Nakamura M (2006) Masculinization of female golden rabbitfish Siganus guttatus using an aromatase inhibitor treatment during sex differentiation. Comp Biochem Physiol C Toxicol Pharmacol 143(4):402–429. doi:10.1016/j.cbpc.2006.04.015

    Article  PubMed  CAS  Google Scholar 

  • Kwon JY, Haghpanah V, Kogson-Hurtado CM, McAndrew BJ, Penman DJ (2000) Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J Exp Zool 287:46–53. doi:10.1002/1097-010X(20000615)287:1<46::AID-JEZ6>3.0.CO;2-X

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Lee FY, Yueh WS, Tacon P, Du JL, Chang CN, Jeng SR, Tanaka H, Chang CF (2000) Profiles of gonadal development, sex steroids, aromatase activity, and gonadotropin II in the controlled sex change of protandrous black porgy, Acanthopagrus schlegeli Bleeker. Gen Comp Endocrinol 119:111–120. doi:10.1006/gcen.2000.7499

    Article  PubMed  CAS  Google Scholar 

  • Liu ZH, Wu FR, Jiao BW, Zhang XY, Hu CJ, Huang BF, Zhou LY, Huang XG, Wang ZJ, Zhang YG, Nagahama Y, Cheng CHK, Wang DS (2007) Molecular cloning of Dmrt1, Foxl2 and Cyp19 in Southern catfish and their possible roles in sex differentiation. J Endocrinol 194:223–241. doi:10.1677/JOE-07-0135

    Article  PubMed  CAS  Google Scholar 

  • Marchand O, Govoroun M, D’Cotta H, McMeel O, Lareyre J, Bernot A, Laudet V, Guiguen Y (2000) DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim Biophys Acta 1493:180–187

    PubMed  CAS  Google Scholar 

  • Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417(6888):559–563. doi:10.1038/nature751

    Article  PubMed  CAS  Google Scholar 

  • Nagahama Y, Kobayashi T, Matsuda M (2004) Sex determination, gonadal sex differentiation and sex change in fish. Tanpakushitsu Kakusan Koso 49(2):116–123

    PubMed  CAS  Google Scholar 

  • Nanda I, Shan Z, Schartl M, Burt DW, Koehler M, Nothwang H, Grutzner F, Paton IR, Windsor D, Dunn I, Engel W, Staeheli P, Mizuno S, Haaf T, Schmid M (1999) 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258–259. doi:10.1038/6769

    Article  PubMed  CAS  Google Scholar 

  • Nanda I, Zend-Ajusch E, Shan Z, Grutzner F, Schartl M, Burt DW, Koehler M, Fowler VM, Goodwin G, Schneider WJ, Mizuno S, Dechant G, Haaf T, Schmid M (2000) Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination. Cytogenet Cell Genet 89:67–78. doi:10.1159/000015567

    Article  PubMed  CAS  Google Scholar 

  • Orn S, Holbech H, Madsen TH, Norrgren L, Petersen GI (2003) Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat Toxicol 65(4):397–411

    PubMed  CAS  Google Scholar 

  • Ottolenghi C, Pelosi E, Tran J, Colombino M, Douglass E, Nedorezov T, Cao A, Forabosco A, Schlessinger D (2007) Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum Mol Genet 16(23):2795–2804. doi:10.1093/hmg/ddm235

    Article  PubMed  CAS  Google Scholar 

  • Pannetier M, Fabre S, Batista F, Kocer A, Renault L, Jolivet G, Mandon-Pepin B, Cotinot C, Veitia R, Pailhoux E (2006) FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J Mol Endocrinol 36:399–413. doi:10.1677/jme.1.01947

    Article  PubMed  CAS  Google Scholar 

  • Patino R, Davis KB, Schoore JE, Uguz C, Strussmann CA, Parker NC, Simco BA, Goudie CA (1996) Sex differentiation of channel catfish gonads: normal development and effect of temperature. J Exp Zool 276:209–218. doi:10.1002/(SICI)1097-010X(19961015)276:3<209::AID-JEZ5>3.0.CO;2-R

    Article  Google Scholar 

  • Piferrer F, Blázquez M, Navarro L, González A (2005) Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 142(1–2):102–110. doi:10.1016/j.ygcen.2005.02.011

    Article  PubMed  CAS  Google Scholar 

  • Raghuveer K, Garhwal R, Wang DS, Bogerd J, Kirubagaran R, Rasheeda MK, Sreenivasulu G, Bhattachrya N, Tarangini S, Nagahama Y, Senthilkumaran B (2006) Effect of methyl testosterone- and ethynyl estradiol-induced sex differentiation on catfish, Clarias gariepinus: expression profiles of DMRT1, cytochrome P450aromatases and 3 β-hydroxysteroid dehydrogenase. Fish Physiol Biochem 31:143–147. doi:10.1007/s10695-006-0016-3

    Article  CAS  Google Scholar 

  • Raymond CS, Parker ED, Kettlewell JR, Brown LG, Page DC, Kusz K, Jaruzelska J, Reinberg Y, Flejter WL, Bardwell VJ, Hirsch B, Zarkower D (1999) A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8:989–996. doi:10.1093/hmg/8.6.989

    Article  PubMed  CAS  Google Scholar 

  • Raymond CS, Murphy MW, O’Sullivan MG, Bardwell VJ, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587–2595. doi:10.1101/gad.834100

    Article  PubMed  CAS  Google Scholar 

  • Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T (2000) Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Cell Genet 89:252–257. doi:10.1159/000015626

    Article  PubMed  CAS  Google Scholar 

  • Sinclair AH, Berta O, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Foodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346(6281):240–244. doi:10.1038/346240a0

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Sinclair AH (2004) Sex determination: insights from the chicken. Bioessays 26:120–132. doi:10.1002/bies.10400

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Katz M, Sinclair AH (2003) DMRT1 is upregulated in the gonads during female-to-male sex reversal in ZW chicken embryos. Biol Reprod 68:560–570. doi:10.1095/biolreprod.102.007294

    Article  PubMed  CAS  Google Scholar 

  • So WK, Kwok HF, Ge W (2005) Zebrafish gonadotropins and their receptors. II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits—their spatial-temporal expression patterns and receptor specificity. Biol Reprod 72(6):1382–1396. doi:10.1095/biolreprod.104.038216

    Article  PubMed  CAS  Google Scholar 

  • Torres MLC, Landa PA, Moreno MN, Marmolejo VA, Meza MA, Merchant LH (2002) Expression profiles of Dax1, Dmrt1, and Sox9 during temperature sex determination in gonads of the sea turtle Lepidochelys olivacea. Gen Comp Endocrinol 129:20–26. doi:10.1016/S0016-6480(02)00511-7

    Article  CAS  Google Scholar 

  • Uchida D, Yamashita M, Kitano T, Iguchi T (2004) An aromatase inhibitor or high water temperature induces oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol 137A:11–20

    CAS  Google Scholar 

  • Vizziano D, Randuineau G, Baron D, Cauty C, Guiguen Y (2007) Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev Dyn 236(8):2198–2206. doi:10.1002/dvdy.21212

    Article  PubMed  CAS  Google Scholar 

  • Vizziano D, Baron D, Randuineau G, Mahè S, Cauty C, Guiguen Y (2008) Rainbow trout gonadal masculinization induced by inhibition of estrogen synthesis is more physiological than masculinization induced by androgen supplementation. Biol Reprod 78:939–946. doi:10.1095/biolreprod.107.065961

    Article  PubMed  CAS  Google Scholar 

  • Wang DS, Kobayashi T, Zhou LY, Nagahama Y (2004) Molecular cloning and gene expression of Foxl2 in the Nile tilapia, Oreochromis niloticus. Biochem Biophys Res Commun 320:83–89. doi:10.1016/j.bbrc.2004.05.133

    Article  PubMed  CAS  Google Scholar 

  • Wang DS, Kobayashi T, Zhou LY, Paul-Prasanth B, Ijiri S, Sakai F, Okubo K, Morohashi K, Nagahama Y (2007) Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol Endocrinol 21:712–725. doi:10.1210/me.2006-0248

    Article  PubMed  CAS  Google Scholar 

  • Wong TT, Zohar Y (2004) Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 145(11):5210–5220. doi:10.1210/en.2004-0558

    Article  PubMed  CAS  Google Scholar 

  • Wu TL (2000) Sex differentiation and temperature-dependent sex determination in Silurus meridionalis Chen. Dissertation, Southwest Normal University of China

  • Wu FR, Zhang XY, Wang DS (2006) Optimal parameters for artificial gynogenesis in Southern catfish. Chin J Zool 41(1):27–31 (in Chinese)

    Google Scholar 

  • Xie XJ, Long TC, Cao ZD (1994) Studies on the composition and growth in the reproductive population of Silurus Meridionalis. J Southwest China Norm Univ 19(1):71–78 (in Chinese)

    Google Scholar 

  • Yu NW, Hsu CY, Ku HH, Chang LT, Liu HW (1993) Gonadal differentiation and secretions of estradiol and testosterone of the ovaries of Rana catesbeiana tadpoles treated with 4-hydroxyandrostenedione. J Exp Zool 265:252–257. doi:10.1002/jez.1402650307

    Article  PubMed  CAS  Google Scholar 

  • Zhang XY (2005) Primary studies on several factors possibly involved in the gonadal sex determination and differentiation of Southern catfish, Silurus meridionalis. Dissertation, Southwest Normal University of China

  • Zhang YG, Xie XJ (1996) Reproductive biology of Silurus Meridionalis Chen: the development and annual change in the gonads. Acta Hydrobiol Sin 20(1):8–17 (in Chinese)

    Google Scholar 

  • Zhang XY, Jiao BW, Wu TL, Jin CB, Wang DS (2005) Histological observation on gonadal sex differentiation in the Southern catfish, Silurus Meridionalis. Chin J Zool 40(1):41–48 (in Chinese)

    Google Scholar 

  • Zhang XY, Liu ZH, Wang DS (2008) Cytological observation on fertilization of Southern catfish, Silurus meridionalis. Sichuan Dong Wu 27(1):7–11 (in Chinese)

    Google Scholar 

  • Zhou LY, Wang DS, Kobayashi T, Yano A, Paul-Prasanth B, Suzuki A, Sakai F, Nagahama Y (2007a) A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney. Endocrinology 148:4282–4291. doi:10.1210/en.2007-0487

    Article  PubMed  CAS  Google Scholar 

  • Zhou LY, Wang DS, Shibata Y, Paul-Prasanth B, Suzuki A, Nagahama Y (2007b) Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka. Biochem Biophys Res Commun 362(3):619–625. doi:10.1016/j.bbrc.2007.08.044

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by grants from the National High Technology Research and Development Program (863 program) of China (No. 2007AA10Z165), the National Natural Science Foundation of China (No. 30770272), the Free Exploration Fund of the Key Laboratory of Eco-environments in the Three Gorges Reservoir Region (Ministry of Education, No. 124470-20500312), the Key Program from the Ministry of Education (No. 2004-104161), Chongqing Natural Science Foundation (No. CSTC2004BB8450), and the Science and Technology Innovation Fund for the Graduates of Southwest University (No. b2007006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. S. Wang.

Additional information

The sequences reported in this article have been deposited in the GenBank database at NCBI and have been assigned the following accession numbers: AAP83133; AAP83132; AY973945; EF015487; AY973947; EF015488; EF015396; AY973946.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Z.H., Zhang, Y.G. & Wang, D.S. Studies on feminization, sex determination, and differentiation of the Southern catfish, Silurus meridionalis—a review. Fish Physiol Biochem 36, 223–235 (2010). https://doi.org/10.1007/s10695-008-9281-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-008-9281-7

Keywords

Navigation