Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Histological study of gonadal development and sex differentiation in Salvelinus fontinalis under Tasmanian climate conditions

Shafaq Fatima A B , Mark Adams A and Ryan Wilkinson A

A National Centre for Marine Conservation and Resource Sustainability, University of Tasmania, Locked Bag 1370, Launceston, Tas. 7250, Australia.

B Corresponding author. Email: sfatima@postoffice.utas.edu.au

Australian Journal of Zoology 59(5) 321-331 http://dx.doi.org/10.1071/ZO11092
Submitted: 17 November 2011  Accepted: 27 February 2012   Published: 20 March 2012

Abstract

This study describes the developmental process of gonads in brook trout from 0 degree days post-hatch (°dph) until completion of sex differentiation (3354°dph). Gonadal development was divided into undifferentiated (0–2013°dph) and differentiated phases (2769–3354°dph). Fertilised eggs (n = 1000) were incubated at 9.5-10°C until hatching at 66 days post-fertilisation (dpf). A total of 20% of alevins sampled on 0°dph were found with unpaired and undifferentiated gonads, indicating that gonadal development commenced before hatch. Initially, undifferentiated gonads contained stromal tissue and few primordial gonadal cells (PGC) (n = 2–5). During the undifferentiated phase, gonads increased in size and proliferative activity of the PGC increased their number (n = 15–22). The differentiated phase commenced with the appearance of sex differentiation at 2769°dph where gonads could be clearly differentiated as ovaries and presumptive testes. Ovaries were identified by the presence of oogonia while presumptive testes contained spermatogonia, vena comittis and a proximal network of cavities. Both ovaries and testes underwent further differentiation until the end of this phase (3354°dph). Oogonia were transformed into primary oocytes while spermatogonial cysts were observed in testes. However, differentiation of steroidogenic cells could not be observed. Direct sex differentiation was found in this study as undifferentiated gonads directly developed into testes and ovaries with anatomical differentiation preceding cytological differentiation. This study confirms previous studies that the prehatch period should be targeted when attempting to produce future monosex populations via indirect sex reversal using androgen treatment.

Additional keywords: brook trout, differentiation, gonadal development.


References

ABARES (2010). Australian Fisheries Statistics. Australian Bureau of Agricultural and Resource Economics and Sciences.

Arezo, M. J., D’Alessandro, S., Papa, N., de Sa, R., and Berois, N. (2007). Sex differentiation pattern in the annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae). Tissue & Cell 39, 89–98.
Sex differentiation pattern in the annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae).CrossRef | 1:STN:280:DC%2BD2s3lslSjtw%3D%3D&md5=d748b8531b871ace81b78f2f97de2ac8CAS | open url image1

Árnason, T., Bjornsson, B., and Steinarsson, A. (2009). Allometric growth and condition factor of Atlantic cod (Gadus morhua) fed to satiation: effects of temperature and body weight. Journal of Applied Ichthyology 25, 401–406.
Allometric growth and condition factor of Atlantic cod (Gadus morhua) fed to satiation: effects of temperature and body weight.CrossRef | open url image1

Baird, H. B., Krueger, C. C., and Josephson, D. C. (2002). Differences in incubation period and survival of embryos among brook trout strains. North American Journal of Aquaculture 64, 233–241.
Differences in incubation period and survival of embryos among brook trout strains.CrossRef | open url image1

Baron, D., Houlgatte, R., Fostier, A., and Guiguen, Y. (2008). Expression profiling of candidate genes during ovary-to-testis trans-differentiation in rainbow trout masculinized by androgens. General and Comparative Endocrinology 156, 369–378.
Expression profiling of candidate genes during ovary-to-testis trans-differentiation in rainbow trout masculinized by androgens.CrossRef | 1:CAS:528:DC%2BD1cXjtlekt7Y%3D&md5=636c96a18682447e619d9c2e11fe8a9eCAS | open url image1

Bascinar, N., Okumubo, U., and Serezlu, R. (2003). The development of brook trout (Salvelinus fontinalis Mitchill, 1814) embryos during the yolk sac period. Turkish Journal of Zoology 27, 227–230. open url image1

Billard, R. (1992). Reproduction in rainbow trout sex differentiation, dynamics of gametogenesis, biology and preservation of gametes. Aquaculture 100, 263–298.
Reproduction in rainbow trout sex differentiation, dynamics of gametogenesis, biology and preservation of gametes.CrossRef | open url image1

Bogdanova, V. A. (2004). Early gametogenesis of the volkhov whitefish, Coregonus lavaretus baeri. Annales Zoologici Fennici 41, 99–104. open url image1

Bull, J. J. (1983). ‘Evolution of Sex Determining Mechanism.’ (Menlo Park: California.)

Cavileer, T., Hunter, S., Okutsu, T., Yoshizaki, G., and Nagler, J. J. (2009). Identification of novel genes associated with molecular sex differentiation in the embryonic gonads of rainbow trout (Oncorhynchus mykiss). Sexual Development: Genetics, Molecular Biology, Evolution, Endocrinology, Embryology, and Pathology of Sex Determination and Differentiation 3, 214–224.
Identification of novel genes associated with molecular sex differentiation in the embryonic gonads of rainbow trout (Oncorhynchus mykiss).CrossRef | 1:CAS:528:DC%2BD1MXhtFarsbrK&md5=124f68c3e3c4db319c526803bb754a92CAS | open url image1

Chiasson, M., and Benfey, T. J. (2007). Gonadal differentiation and hormonal sex reversal in arctic charr (Salvelinus alpinus). Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology 307A, 527–534.
Gonadal differentiation and hormonal sex reversal in arctic charr (Salvelinus alpinus).CrossRef | 1:CAS:528:DC%2BD2sXhtVOrsb3N&md5=6ff36fd3eeb381acaac797d193415819CAS | open url image1

Chiasson, M., Benfey, T. J., and Martin-Robichaud, D. J. (2008). Gonadal differentiation in Atlantic cod, Gadus morhua L., and haddock, Melanogrammus aeglefinus (L.). Acta Ichthyologica et Piscatoria 38, 127–133.
Gonadal differentiation in Atlantic cod, Gadus morhua L., and haddock, Melanogrammus aeglefinus (L.).CrossRef | open url image1

Clements, J. (1988). ‘Salmon at the antipodes: a history and review of trout, salmon and char and introduced coarse fish in Australasia.’ (Alfredton: Ballarat, Vic.)

Devlin, R. H., and Nagahama, Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191–364.
Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences.CrossRef | 1:CAS:528:DC%2BD38XktFKjsbY%3D&md5=50a9ec029ba08880d741c9cbf934ac7dCAS | open url image1

Dlugosz, M., and Demska Zakes, K. (1989). Sex differentiation in whitefish (Coregonus lavaretus L.). Acta Ichthyologica et Piscatoria 19, 1989. open url image1

Dziewulska, K., and Domagala, J. (2004). Testicular development in the sea trout (Salmo trutta morpha trutta L.) after sex differentiation, with a reference to precocious maturation. Journal of Applied Ichthyology 20, 282–289.
Testicular development in the sea trout (Salmo trutta morpha trutta L.) after sex differentiation, with a reference to precocious maturation.CrossRef | open url image1

Feist, G., Schreck, C. B., Fitzpatrick, M. S., and Redding, J. M. (1990). Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. General and Comparative Endocrinology 80, 299–313.
Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation.CrossRef | 1:CAS:528:DyaK3cXmt1yiu7w%3D&md5=b0d6a4d7eb5e87d3d2e8078100e79625CAS | open url image1

Fitzpatrick, M. S., Feist, G., Redding, J. M., and Schreck, C. B. (1987). Whole body steroid content and in vitro steroid secretion during sexual differentiation in salmonids. In ‘Third International Symposium of Reproductive Physiology of Fish’. p. 130. (St Johns, Canada.)

Fitzpatrick, M. S., Pereira, C. B., and Schreck, C. B. (1993). In vitro steroid secretion during early development of mono sex rainbow trout sex differences, onset of pituitary control, and effects of dietary steroid treatment. General and Comparative Endocrinology 91, 199–215.
In vitro steroid secretion during early development of mono sex rainbow trout sex differences, onset of pituitary control, and effects of dietary steroid treatment.CrossRef | 1:CAS:528:DyaK3sXmt1ahsL8%3D&md5=5d732b3659aa71ec41e1727021391e95CAS | open url image1

Foyle, J. P. (1993). A histological description of gonadal development and sex differentiation in the coho salmon (Oncorhynchus kisutch) for both untreated and oestradiol immersed fry. Journal of Fish Biology 42, 699–712.
A histological description of gonadal development and sex differentiation in the coho salmon (Oncorhynchus kisutch) for both untreated and oestradiol immersed fry.CrossRef | 1:CAS:528:DyaK3sXlsFKls7w%3D&md5=86ca95cba2bf8cc388403fbeef513891CAS | open url image1

Froese, R. (2006). Cube law, condition factor and weight length relationships: history, meta analysis and recommendations. Journal of Applied Ichthyology 22, 241–253.
Cube law, condition factor and weight length relationships: history, meta analysis and recommendations.CrossRef | open url image1

Galbreath, P., Adams, N., and Sherrill, L. (2003). Successful sex reversal of brook trout with 17 alpha-methyldihydrotestosterone treatments. North American Journal of Aquaculture 65, 235–239.
Successful sex reversal of brook trout with 17 alpha-methyldihydrotestosterone treatments.CrossRef | open url image1

Haffray, P., Petit, V., Guiguen, Y., Quillet, E., Rault, P., and Fostier, A. (2009). Successful production of monosex female brook trout Salvelinus fontinalis using gynogenetic sex reversed males by a combination of methyltestosterone immersion and oral treatments. Aquaculture 290, 47–52.
Successful production of monosex female brook trout Salvelinus fontinalis using gynogenetic sex reversed males by a combination of methyltestosterone immersion and oral treatments.CrossRef | 1:CAS:528:DC%2BD1MXktF2ltr4%3D&md5=e9a1cb249e2edb2fe85ee1b86143aa9fCAS | open url image1

Hartley, S. E. (1987). The chromosomes of salmonid fishes. Biological Reviews of the Cambridge Philosophical Society 62, 197–214.
The chromosomes of salmonid fishes.CrossRef | open url image1

Horobin, R. W. (2002). ‘Theory and Practice of Histological Techniques.’ (Churchill Livingstone: London.)

Kanamori, A., Nagahama, Y., and Egami, N. (1985). Development of the tissue architecture in the gonads of the medaka Oryzias latipes. Zoological Science 2, 695–706. open url image1

Krol, J., Demska-Zakes, K., Hliwa, P., and Korzeniowska, G. (2003). Influence of temperature on the sex differentiation process in peled Coregonus peled (Gmel.). Archives of Polish Fisheries 11, 23–31. open url image1

Laird, L. M., Ellis, A. E., Wilson, A. R., and Holliday, F. G. T. (1978). The development of the gonadal and immune systems in the Atlantic salmon (Salmo salar L.) and a consideration of the possibility of inducing autoimmune destruction of the testis. Annales de Biologie Animale, Biochimie, Biophysique 18, 1101–1106. open url image1

Lebrun, C., Billard, R., and Jalabert, B. (1982). Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the 1st 10 post hatching weeks. Reproduction, Nutrition, Development 22, 405–412.
Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the 1st 10 post hatching weeks.CrossRef | 1:STN:280:DyaL3s7hvV2ksQ%3D%3D&md5=62a7b2d45d90b0e1945a35e7df86cb1eCAS | open url image1

Lee, G. M., and Wright, J. E. (1981). Mitotic and meiotic analyses of brook trout, Salvelinus fontinalis. The Journal of Heredity 72, 321–327. open url image1

Marten, P. S. (1992). Effect of temperature-variation on the incubation and development of brook trout eggs. Progressive Fish-Culturist 54, 1–6.
Effect of temperature-variation on the incubation and development of brook trout eggs.CrossRef | open url image1

McMillan, D. B. (2007). ‘Fish Histology: Female Reproductive Systems.’ (Springer: Dordrecht, The Netherlands.)

Nakamura, M. (1978). Morphological and experimental studies on sex differentiation of the gonad in several teleost fishes. Hokkaoido University, Hokkaoido, Japan.

Nakamura, M. (1982). Gonadal sex differentiation in whitespotted char, Salvelinus leucomaenis. Japanese Journal of Ichthyology 28, 431–436. open url image1

Nakamura, M., and Nagahama, Y. (1985). Steroid producing cells during ovarian differentiation of the tilapia, Sarotherodon niloticus. Development, Growth & Differentiation 27, 701–708.
Steroid producing cells during ovarian differentiation of the tilapia, Sarotherodon niloticus.CrossRef | open url image1

Nakamura, M., and Nagahama, Y. (1989). Differentiation and development of Leydig cells, and changes of testosterone levels during testicular differentiation in tilapia Oreochromis niloticus. Fish Physiology and Biochemistry 7, 211–219.
Differentiation and development of Leydig cells, and changes of testosterone levels during testicular differentiation in tilapia Oreochromis niloticus.CrossRef | 1:CAS:528:DyaL1MXlvFWrs7k%3D&md5=497ef6feb088983c144120b801b223c8CAS | open url image1

Nakamura, M., and Nagahama, Y. (1993). Ultrastructural study on the differentiation and development of steroid producing cells during ovarian differentiation in the amago salmon, Oncorhynchus rhodurus. Aquaculture 112, 237–251.
Ultrastructural study on the differentiation and development of steroid producing cells during ovarian differentiation in the amago salmon, Oncorhynchus rhodurus.CrossRef | 1:CAS:528:DyaK3sXksVGksL4%3D&md5=128dfee9be075feae237b3cfe96737fbCAS | open url image1

Nakamura, H., Takahashi, H., and Hiroi, O. (1974). Sex differentiation of the gonad in the masu salmon (Oncorhynchus masou). Scientific Reports of the Hokkaido Fish Hatchery 28, 1–8. open url image1

Nakamura, M., Kobayashi, T., Chang, X. T., and Nagahama, Y. (1998). Gonadal sex differentiation in teleost fish. The Journal of Experimental Zoology 281, 362–372.
Gonadal sex differentiation in teleost fish.CrossRef | open url image1

Ovenden, J. R., Bywater, R., and White, R. W. G. (1993). Mitochondrial-DNA nucleotide-sequence variation in atlantic salmon (Salmo salar), brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis) from Tasmania, Australia. Aquaculture 114, 217–227.
Mitochondrial-DNA nucleotide-sequence variation in atlantic salmon (Salmo salar), brown trout (Salmo trutta), rainbow trout (Oncorhynchus mykiss) and brook trout (Salvelinus fontinalis) from Tasmania, Australia.CrossRef | 1:CAS:528:DyaK3sXlslOrurg%3D&md5=e720bf078b777b954c5840b7a8a9a973CAS | open url image1

Penman, D. J., and Piferrer, F. (2008). Fish gonadogenesis. Part I: Genetic and environmental mechanisms of sex determination. Reviews in Fisheries Science 16, 16–34.
Fish gonadogenesis. Part I: Genetic and environmental mechanisms of sex determination.CrossRef | 1:CAS:528:DC%2BD1cXhtFeitLzO&md5=e70cd78e689a53909a9f0bbcc92bab1eCAS | open url image1

Phillips, R. B., Matsuoka, M. P., and Reed, K. M. (2002). Characterization of charr chromosomes using fluorescence in situ hybridization. Environmental Biology of Fishes 64, 223–228.
Characterization of charr chromosomes using fluorescence in situ hybridization.CrossRef | open url image1

Piferrer, F. (2001). Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197, 229–281.
Endocrine sex control strategies for the feminization of teleost fish.CrossRef | 1:CAS:528:DC%2BD3MXjsFalsbk%3D&md5=d898151935616fb89bedebc978dd5c97CAS | open url image1

Piferrer, F., and Donaldson, E. M. (1989). Gonadal differentiation in coho salmon, Oncorhynchus kisutch, after a single treatment with androgen or estrogen at different stages during ontogenesis. Aquaculture 77, 251–262. open url image1

Piferrer, F., and Guiguen, Y. (2008). Fish gonadogenesis. Part II: Molecular biology and genomics of sex differentiation. Reviews in Fisheries Science 16, 35–55.
Fish gonadogenesis. Part II: Molecular biology and genomics of sex differentiation.CrossRef | 1:CAS:528:DC%2BD1cXhtFeitL%2FN&md5=1e06a6593dd846c42772a823ac6c40ccCAS | open url image1

Robertson, J. B. (1953). Sex differentiation in the Pacific salmon Onchorhynchus keta (Walbaum). Canadian Journal of Zoology 31, 73–79.
Sex differentiation in the Pacific salmon Onchorhynchus keta (Walbaum).CrossRef | open url image1

Sacobie, C. F. D., and Benfey, T. J. (2005). Sex differentiation and early gonadal development in brook trout. North American Journal of Aquaculture 67, 181–186.
Sex differentiation and early gonadal development in brook trout.CrossRef | open url image1

Sandra, G. E., and Norma, M. M. (2010). Sexual determination and differentiation in teleost fish. Reviews in Fish Biology and Fisheries 20, 101–121.
Sexual determination and differentiation in teleost fish.CrossRef | open url image1

Schreibman, M. P., Berkowitz, E. J., and van den Hurk, R. (1982). Histology and histochemistry of the testis and ovary of the platyfish, Xiphophorus maculatus, from birth to sexual maturity. Cell and Tissue Research 224, 81–87.
Histology and histochemistry of the testis and ovary of the platyfish, Xiphophorus maculatus, from birth to sexual maturity.CrossRef | 1:CAS:528:DyaL38Xkt1WjtbY%3D&md5=37da2aab70f487b30904e1bdc26dd69cCAS | open url image1

Strüssmann, C. A., and Nakamura, M. (2002). Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiology and Biochemistry 26, 13–29.
Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes.CrossRef | open url image1

Takashima, F., Patino, R., and Nomura, M. (1980). Histological studies on the sex differentiation in rainbow trout. Bulletin of the Japanese Society of Scientific Fisheries 46, 1317–1322.
Histological studies on the sex differentiation in rainbow trout.CrossRef | open url image1

Tanaka, M., Saito, D., Morinaga, C., and Kurokawa, H. (2008). Cross talk between germ cells and gonadal somatic cells is critical for sex differentiation of the gonads in the teleost fish, medaka (Oryzias latipes). Development, Growth & Differentiation 50, 273–278.
Cross talk between germ cells and gonadal somatic cells is critical for sex differentiation of the gonads in the teleost fish, medaka (Oryzias latipes).CrossRef | open url image1

van den Hurk, R., and Slof, G. A. (1981). A morphological and experimental study of gonadal sex differentiation in the rainbow trout, Salmo gairdneri. Cell Tissue Research 218, 487–497.
| 1:CAS:528:DyaL3MXkvFCisbo%3D&md5=8a190834999e8008b0468438b415b5e3CAS | open url image1

van den Hurk, R., Lambert, J. G. D., and Peute, J. (1982). Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiation. Reproduction, Nutrition, Development 22, 413–425.
Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiation.CrossRef | 1:CAS:528:DyaL38Xks12lt7g%3D&md5=edf603e8fd223c99d70870c4461f8a22CAS | open url image1

von Schalburg, K. R., Yasuike, M., Yazawa, R., de Boer, J. G., Reid, L., So, S., Robb, A., Rondeau, E. B., Phillips, R. B., Davidson, W. S., and Koop, B. F. (2011). Regulation and expression of sexual differentiation factors in embryonic and extragonadal tissues of Atlantic salmon. BMC Genomics 12, 31.
| 1:CAS:528:DC%2BC3MXhtFOhu7c%3D&md5=210d63b5abcc28e7b18361652a377e16CAS | open url image1

Wenstrom, J. C. (1975). ‘Sex differentiation and hormone directed sex determination in the lake trout (Salvelinus namaycush).’ (Northern Michigan University: Marquette, MI.)

Yamamoto, T. (1969). ‘Fish Physiology.’ (Academic Press: New York.)



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