Skip to main content
SpringerLink
Log in

Gonadogenesis analysis and sex differentiation in cultured turbot (Scophthalmus maximus)

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

Abstract

As a flatfish, the turbot (Scophthalmus maximus) is one of the most important farmed fish species with great commercial value, which has a strong sexual dimorphism on growth rate and sexual maturity. In this study, using histology, the basic information on proliferation and migration of germ cells and early gonadal development during sex differentiation in turbot were described in detail. There were six to nine individual primordial germ cells (PGCs) with large nuclei until 15 days post-hatching (dph). The PGCs located under the mesonephric ducts undergo migration along the dorsal mesentery toward the region of the genital ridge from 0 to 15 dph. During migration, the number of PGCs was constant, and the expression of vasa had no significant changes. At 20 dph, the aggregation of somatic cells at genital ridge indicated the formation of primary gonad. Furthermore, the number of PGCs was increased to 60 and the expression of vasa was upregulated for the first time. The undifferentiated gonads with no morphological indications of sex differentiation grew larger with the increase in germ cells and somatic cells number/size from 20 to 35 dph. During 36–52 dph, cytological gonadal differentiation was observed. In presumptive testes of type I gonadal tissue (with a lance shape), the number of germ cells increased steadily and the germ cells had the same characteristics as before. Meanwhile, in presumptive ovaries of type II gonadal tissue (with a club-like shape), the germ cells proliferated and induced in two different populations of germ cells. One type had the morphological characteristics as undifferentiated germ cells, while the other type of germ cells underwent mitosis exhibiting smaller size and mottled nuclei. At 60 dph, ovarian cavity was present in the gonad of type II, which would develop into ovaries. However, spermatogonial cysts were not noticed in the gonad of type I until 90 dph, which indicated the formation of the testes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Arezo MJ, D’Alessandro S, Papa N, de Sá R, Berois N (2007) Sex differentiation pattern in the annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae). Tissue Cell 39:89–98

    Article  CAS  PubMed  Google Scholar 

  • Chiasson M, Benfey TJ (2007) Gonadal differentiation and hormonal sex reversal in Arctic charr (Salvelinus alpinus). J Exp Zool Part A Ecol Genet Physiol 307:527–534

    Article  Google Scholar 

  • Dai XY, Jin X, Chen XW, He JY, Yin Z (2015) Sufficient numbers of early germ cells are essential for female sex development in zebrafish. PLoS ONE 10:15. doi:10.1371/journal.pone.0117824

    Google Scholar 

  • Deniz Koç N, Yüce R (2012) A light- and electron microscopic study of primordial germ cells in the zebra fish (Danio rerio). Biol Res 45:331–336

    Article  PubMed  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • Fairchild EA, Rennels N, Howell WH, Wells RE (2007) Gonadal development and differentiation in cultured juvenile winter flounder, Pseudopleuronectes americanus. J World Aquac Soc 38:8

    Article  Google Scholar 

  • Fatima S, Adams M, Wilkinson R (2011) Histological study of gonadal development and sex differentiation in Salvelinus fontinalis under Tasmanian climate conditions. Aust J Zool 59:321. doi:10.1071/zo11092

    Article  Google Scholar 

  • FEAP (2015) European aquaculture production report 2005–2014. Federation of European Aquaculture Producers. http://www.feap.info/Default.asp?SHORTCUT=582. Accessed 20 Aug 2015

  • Foyle TP (1993) A histological description of gonadal development and sex differentiation in the coho salmon (Oncorhynchus kisutch) for both untreated and oestradiol immersed fry. J Fish Biol 42:699–712

    Article  CAS  Google Scholar 

  • Gao Z et al (2009) Gonadal sex differentiation in the bluegill sunfish Lepomis macrochirus and its relation to fish size and age. Aquaculture 294:138–146

    Article  Google Scholar 

  • Guerrero SM, Moreno-Mendoza N (2009) Gonadal sex differentiation in Chapalichthys encaustus (Teleostei: Goodeidae). Dev Biol 331:443

    Article  Google Scholar 

  • Haffray P, Lebègue E, Jeu S, Guennoc M, Guiguen Y, Baroiller JF, Fostier A (2009) Genetic determination and temperature effects on turbot Scophthalmus maximus sex differentiation: an investigation using steroid sex-inverted males and females. Aquaculture 294:30–36

    Article  Google Scholar 

  • Hamaguchi S (1982) A light- and electron-microscopic study on the migration of primordial germ cells in the teleost, Oryzias latipes. Cell Tissue Res 227:139–151. doi:10.1007/BF00206337

    Article  CAS  PubMed  Google Scholar 

  • Hendry CI, Martin-Robichaud DJ, Benfey TJ (2002) Gonadal sex differentiation in Atlantic halibut. J Fish Biol 60:1431–1442

    Article  Google Scholar 

  • Kobayashi T, Ishibashi R, Yamamoto S, Otani S, Ueno K, Murata O (2011) Gonadal morphogenesis and sex differentiation in cultured chub mackerel, Scomber japonicus. Aquac Res 42:230–239

    Article  Google Scholar 

  • Lebrun C, Billard R, Jalabert B (1982) Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the first 10 post-hatching weeks. Reprod Nutr Dév 22:405–412

    Article  CAS  PubMed  Google Scholar 

  • Lei J (2003) The development direction of turbot farming industry in China. Sci Fish Farm 7:3–4 (in Chinese)

    Google Scholar 

  • Lewis ZR, McClellan MC, Postlethwait JH, Cresko WA, Kaplan RH (2008) Female-specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus). J Morphol 269:909–921

    Article  PubMed  Google Scholar 

  • Lin F et al (2012) Germ line specific expression of a vasa homologue gene in turbot (Scophthalmus maximus): evidence for vasa localization at cleavage furrows in euteleostei. Mol Reprod Dev 79:803–813

    Article  CAS  PubMed  Google Scholar 

  • Luckenbach JA, Godwin J, Daniels HV, Borski RJ (2003) Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma). Aquaculture 216:13

    Article  Google Scholar 

  • Mandich A, Massari A, Bottero S, Marino G (2002) Histological and histochemical study of female germ cell development in the dusky grouper Epinephelus marginatus (Lowe, 1834). Eur J Histochem 46:87–100

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y (1983) The Functional-morphology of teleost gonads. Fish Physiol 9:223–275

    Article  CAS  Google Scholar 

  • Nagai T, Yamaha E, Arai K (2001) Histological differentiation of primordial germ cells in zebrafish. Zool Sci 18:215–223

    Article  Google Scholar 

  • Nakamura M, Kobayashi T, Chang X-T, Nagahama Y (1998) Gonadal sex differentiation in teleost fish. J Exp Zool 281:362–372

    Article  Google Scholar 

  • Nishimura T, Tanaka M (2014) Gonadal development in fish. Sex Dev 8:252–261

    Article  PubMed  Google Scholar 

  • Orban L, Sreenivasan R, Olsson PE (2009) Long and winding roads: testis differentiation in zebrafish. Mol Cell Endocrinol 312:35–41

    Article  CAS  PubMed  Google Scholar 

  • Parmentier HK, Timmermans LPM (1985) The differentiation of germ cells and gonads during development of carp (Cyprinus carpio L.). A study with anti-carp sperm monoclonal antibodies. J Embryol Exp Morphol 90:13–32

    CAS  PubMed  Google Scholar 

  • Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197:229–281

    Article  CAS  Google Scholar 

  • Raz E (2003) Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet 4:690–700

    Article  CAS  PubMed  Google Scholar 

  • Sacobie CFD, Benfey TJ (2005) Sex differentiation and early gonadal development in brook trout. N Am J Aquac 67:181–186

    Article  Google Scholar 

  • Saito D et al (2007) Proliferation of germ cells during gonadal sex differentiation in medaka: insights from germ cell-depleted mutant zenzai. Dev Biol 310:280–290

    Article  CAS  PubMed  Google Scholar 

  • Sandra G-E, Norma M-M (2009) Sexual determination and differentiation in teleost fish. Rev Fish Biol Fish 20:101–121

    Article  Google Scholar 

  • Satoh N, Egami N (1972) Sex differentiation of germ cells in the teleost, Oryzias latipes, during normal embryonic development. J Embryol Exp Morphol 28:385–395

    CAS  PubMed  Google Scholar 

  • Takashima F, Patino R, Nomura M (1980) Histological studies on the sex differentiation in rainbow. Bull Jpn Soc Sci Fish 46:1317–1322

    Article  Google Scholar 

  • Timmermans LPM, Taverne N (1989) Segregation of primordial germ cells: their numbers and fate during early development of Barbus conchonius (Cyprinidae, Teleostei) as indicated by 3H-thymidine incorporation. J Morphol 202:225–237

    Article  Google Scholar 

  • Uchida D, Yamashita M, Kitano T, Iguchi T (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205:711–718

    PubMed  Google Scholar 

  • Uguz C, Iscan M, Togan I (2003) Developmental genetics and physiology of sex differentiation in vertabrates. Environ Toxicol Pharmacol 14:9–16

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto T-O (1969) 3 Sex differentiation. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 3. Academic Press, New York, pp 117–175

    Google Scholar 

  • Yamamoto E (1999) Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173:235–246. doi:10.1016/S0044-8486(98)00448-7

    Article  Google Scholar 

  • Yvan F et al (1983) La gonadogenèse des Poissons. Reprod Nutr Dev 23:453–491

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by National Natural Science Foundation of China (Nos. 31372514, 31472264, 31572602), Modern Agro-Industry Technology Research System (nycytx-50), China Postdoctoral Science Foundation (2014M551973), the Scientific and Technological Innovation Project Financially Supported by Qingdao National Laboratory for Marine Science and Technology (Nos. 2015ASKJ02, 2015ASKJ02-03-03), Youth Innovation Promotion Association CAS and Chinese Academy of Science and Technology Service Network Planning (KFJ-EW-STS-060).

Author information

Authors and Affiliations

  1. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Chunyan Zhao, Shihong Xu, Yifan Liu, Yanfeng Wang, Qinghua Liu & Jun Li

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Chunyan Zhao

  3. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Chunyan Zhao, Shihong Xu, Yifan Liu, Yanfeng Wang, Qinghua Liu & Jun Li

Authors
  1. Chunyan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shihong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yifan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qinghua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qinghua Liu or Jun Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, C., Xu, S., Liu, Y. et al. Gonadogenesis analysis and sex differentiation in cultured turbot (Scophthalmus maximus). Fish Physiol Biochem 43, 265–278 (2017). https://doi.org/10.1007/s10695-016-0284-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0284-5

Keywords

Search

Navigation