Spermatogenesis in the yellowtail tetra Astyanax altiparanae: a histological analyses with emphasis to spermatogonial and spermatid types
Keywords:
fish reproduction, germ cells, spermiogenesis, testis morphologyAbstract
This study aimed at the detailed description of the characteristics of the different germ cell types found in Astyanax altiparanae during spermatogenesis. In this purpose, testes from 25 adult male specimens of A. altiparanae were sampled and submitted to the usual techniques of light microscopy. Based on nuclear shape, chromatin condensation, nucleoli quantity and cell size, four spermatogonial types were identified: type A undifferentiated (Aund.*); type A undifferentiated (Aund.); type A differentiated (Adif.); and type B spermatogonia. Spermatocytes were observed in different phases of meiosis (leptotene/zygotene/pachytene and diplotene), metaphase I and II and secondary spermatocytes, being distinguish mainly by their chromosomal organization inside the nucleus. It was also identified three different types of spermatids, which were named as initial, intermediate and final, which can be differentiated by increase in nuclear condensation and spacing among cells inside the cysts, possibly by flagella arise and reduction in nuclear diameter. Thus, this study contribute to a better understand of spermatogenesis in this and other fish species.
References
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the number of mitotic divisions in fish testes. Fisheries Science, 66(2): 299-303.
ALEXANDRINO, A.C.; PHAN, M.T.; PINHEIRO,E.F.G. 1985 Caracterização macroscópica e
microscópica das gônadas do curimbatá,Prochilodus scrofa (Steindachner, 1881), durante o
ciclo reprodutivo. Boletim de Zoologia, 9: 159-175.
BILLARD, R. 1984 Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia
reticulata during spermatogenesis. Cell Tissue Research, 237(2): 219-226.
BRUSLÉ, S. 1981 Ultrastructure of spermiogenesis in Liza aurata Risso, 1810 (Teleostei, Mugilidae).
Cell Tissue Research, 217(2): 415-424.
CASTILHO-ALMEIDA, R.B. 2007 Astyanax altiparanae (Pisces, Characiformes) como modelo
biológico de espécie de peixe para exploração zootécnica e biomanipulação. Botucatu. 119p.
(Doctoral Thesis. Universidade Estadual Paulista - UNESP). Available at: <http://www.ibb.unesp.
br/posgrad/teses/zoologia_do_2007_rodrigo_almeida.pdf> Access on: 20 Nov. 2014.
DE BEM, J.C. 2009 Desenvolvimento gonadal inicial e reversão sexual em Astyanax altiparanae (Teleostei,Characidae). Rio Claro. 96p. (Masters Dissertation.Universidade Estadual Paulista - UNESP).Available at: <http://repositorio.unesp.br/bitstream/handle/11449/87742/bem_jc_me_rcl
a.pdf?sequence=1&isAllowed=y> Access on: 20 Nov. 2014.
DE ROOIJ, D.G. and RUSSELL, L.D. 2000 All you wanted to know about spermatogonia but were
afraid to ask. Journal of Andrology, 21(6): 776-798.
GARUTTI, V. and BRITSKI, H.A. 2000 Descrição de uma espécie nova de Astyanax (Teleostei:
Characidae) da bacia do alto Rio Paraná e considerações gerais sobre as demais espécies do
gênero na bacia. Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, 13:
65-88.
GRIER, H.J.; LINTON, J.R.; LEATHERLAND, J.F.; VLAMING, V.L. 1980 Structural evidence for
two different testicular types in Teleost fishes. The American Journal of Anatomy, 159(3): 331-345.
GRIER, H.J. and ARANZÁBAL, M.C.U. 2009 The testis and spermatogenesis in Teleosts. In:
JAMIESON, B.G.M. Reproductive Biology and Phylogeny of Fishes: Agnathans and Bony Fishes, 8.
St. Lucia: University of Queensland Press.p.119-142.
QUAGIO-GRASSIOTTO, I.; GAMIERO, M.C.;SCHNEIDER, T.; MALABARBA, L.R.; OLIVEIRA,C. 2003 Spermiogenesis and spermatozoa ultrastructure in five species of the Curimatidae with some considerations of spermatozoa ultrastructure in the Characiformes. Neotropical Ichthyology, 1(1): 35-45
JAMIESON, B.G.M. 1991 Fish Evolution and Systematics: Evidence from spermatozoa.
Cambridge: Cambridge University Press. 319p.
LEAL, M.C.; CARDOSO, E.R.; NOBREGA, R.H.;BATLOUNI, S.R.; BOGERD, J.; FRANí"¡A, L.R.; SCHULZ, R.W. 2009 Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biology of Reproduction, 81(1): 77-187.
LO NOSTRO, F.; GRIER, H.; GUERRERO, G.A. 2003 Involvement of the gonadal germinal epithelium
during sex reversal and seasonal testicular cycling in the protogynous swamp eel,Synbranchus marmoratus Bloch 1795 (Teleostei,Synbranchidae). Journal of Morphology, 257(1):107-126.
LOPES, D.C.J.R.; BAZZOLI, N.; BRITO, M.F.G.;MARIA, T.A. 2004 Male reproductive apparatus
in the South American catfish Conorhynchus conirostris. Journal of Fish Biology, 64(5): 1419-1424.
MAZZOLDI, C.; LORENZI, V.; RASOTTO, M.B. 2007 Variation of male reproductive apparatus in
relation to fertilization modalities in the catfish families Auchenipteridae and Callichthyidae
(Teleostei: Siluriformes). Journal of Fish Biology,70(1): 243-256.
MORENA, A.R.; BOITANI, C.; PESCE, M.; FELICI,M.; STEFANINI M. 1996 Isolation of Highly
Purified Type A Spermatogonia From Prepubertal Rat Testis. Journal of Andrology,17(6): 708-717.
NÓBREGA, R.H.; LO NOSTRO, F.L.; GRIER, HARRY, J.; QUAGIO-GRASSIOTTO, I. 2006 Cellular proliferation in fish male germinal epithelium. In: INTERNATIONAL SYMPOSIUM ON ANIMAL BIOLOGY OF REPRODUCTION -From sex differentiation to reproductive biotechnology. Animal Reproduction, 3: 199-199.
NÓBREGA, R.H.; LACERDA, S.M.N.S.; COSTA, G.M.J.; SILVA, R.C.; SCHULZ, R.W.; FRANí"¡A,
L.R. 2008 Development of germ cell transplantation in zebrafish (Danio rerio): a means to study the spermatogonial stem cells in fish. In: INTERNATIONAL SYMPOSIUM ON ANIMAL BIOLOGY OF REPRODUCTION, 2.,São Paulo, 19-22/Nov./2008. Anais… São Paulo:Brazilian College of Animal Reproduction.
NÓBREGA, R.H.; BATLOUNI, S.R.; FRANí"¡A, L.R.2009 An overview of functional and stereological
evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiology
Biochemistry, 35(1): 197-206.
NÓBREGA, R.H.; GREEBE, C.; DE KANT, H.V.; BOGERD J.; FRANí"¡A, L.R.; SCHULZ, R.W. 2010 Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PlosOne, 5(9): e12808. [on line] doi:10.1371/journal.pone.0012808
ORSI, M.L.; SHIBATTA, O.A.; SILVA-SOUZA, A.T.2002 Caracterização biológica de populações de
peixes do rio Tibagi, localidade de Sertanópolis. In: MEDRI, M.E.; BIANCHINI, E.; SHIBATTA,
O.A.; PIMENTA, J.A. A bacia do rio Tibagi. Londrina: Universidade Estadual de Londrina.
p.425-432.
REIS, R.E.; KULLANDER, S.O.; FERRARIS JR, C.J. 2003 Check list of the freshwater fishes of South and
Central America. Porto Alegre: PUCRS Press. 742p.
ROOSE-RUNGE, E.C. 1962 The process of spermatogenesis in mammals. Biological Reviews,
37(3): 343-377.
RUSSELL, L.D.; ETTLIN, R.A.; SINHA HIKIM, A.P.;CLEGG, E.D. 1990 Mammalian spermatogenesis.
Histological and histopathological evaluation of the testis. Clearwater: Cache River Press. 40p.
SCHULZ, R.W.; MENTING, S.; BOGERD, J.;FRANí"¡A, L.R.; VILELA, D.A.R; GODINHO, H.P. 2005 Sertoli cell proliferation in the adult testis: evidence from two fish species belonging to different orders. Biology of Reproduction, 73(5):891-898.
SCHULZ, R.W.; FRANí"¡A, L.R.; LAREYRE, J.J.;LEGAC, F.; CHIARINI-GARCIA, H.; NOBREGA, R.H.; MIURA, T. 2010 Spermatogenesis in fish. General and Comparative Endocrinology, 165(3): 390-411.
SILVA, M. 1987 Morfologia ultra-estrutural do testículo,cinética da espermatogênese e barreira hemotesticular da tilápia do Nilo, Oreochromis niloticus. Belo Horizonte. 164p. (Doctoral Thesis. Universidade Federal de Minas Gerais - UFMG).
SIQUEIRA-SILVA, D.H.; DA-SILVA-COSTA, R.; NINHAUS-SILVEIRA, A.; VICENTINI, C.A.;VERÍSSIMO-SILVEIRA, R. 2012 Ultrastructural analysis of spermiogenesis in the neotropical cichlid Kullander & Ferreira, 2006 (Perciformes:Cichlidae). Journal of Applied Ichthyology, 28(6):878-882.
SIQUEIRA-SILVA, D.H.D.; VICENTINI, C.A.;NINHAUS-SILVEIRA, A.; VERISSIMO-SILVEIRA, R. 2013 Reproductive cycle of the Neotropical cichlid yellow peacock bass Cichla kelberi: A novel pattern of testicular development. Neotropical Ichthyology, 11(3): 587-596.
VAZZOLER, A.E.A.M. 1996 Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem. 169p.
VERÍSSIMO-SILVEIRA, R.; GUSMÃO-POMPIANI,P.; VICENTINI, C.A.; QUAGIO-GRASSIOTTO,I. 2006 Spermiogenesis and spermatozoa ultrastructure in Salminus and Brycon, two primitive genera in Characidae (Teleostei:Ostariophysi: Characiformes). Acta Zoologica,87(4): 305-313.
VILELA, D.A.R.; SILVA, S.G.B.; PEIXOTO, M.T.D.;GODINHO, H.P.; FRANí"¡A, L.R. 2003 Spermatogenesis in teleost: insights from the Nile tilapia (Oreochromis niloticus) model. Fish
Physiology and Biochemistry, 28(1): 187-190.
VERGÍLIO, C.S.; MOREIRA, R.V.; CARVALHO,C.E.V.; MELO, E.J.T. 2012 Characterization of
mature testis and sperm morphology of Gymnotus carapo (Gymnotidae, Teleostei) from
the southeast of Brazil. Acta Zoologica, 0: 1-7.
YASUI, G.S.; SANTOS, M.P.; NAKAGHI, L.S.O.;SENHORINI, J.A.; ARIAS-RODRIGUEZ, L.; FUJIMOTO, T.; SHIMODA, E.; SILVA, L.A. 2014 Improvement of gamete quality and its shortterm storage: an approach for biotechnology in laboratory fish. Animal, 9(3): 464-470.
the number of mitotic divisions in fish testes. Fisheries Science, 66(2): 299-303.
ALEXANDRINO, A.C.; PHAN, M.T.; PINHEIRO,E.F.G. 1985 Caracterização macroscópica e
microscópica das gônadas do curimbatá,Prochilodus scrofa (Steindachner, 1881), durante o
ciclo reprodutivo. Boletim de Zoologia, 9: 159-175.
BILLARD, R. 1984 Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia
reticulata during spermatogenesis. Cell Tissue Research, 237(2): 219-226.
BRUSLÉ, S. 1981 Ultrastructure of spermiogenesis in Liza aurata Risso, 1810 (Teleostei, Mugilidae).
Cell Tissue Research, 217(2): 415-424.
CASTILHO-ALMEIDA, R.B. 2007 Astyanax altiparanae (Pisces, Characiformes) como modelo
biológico de espécie de peixe para exploração zootécnica e biomanipulação. Botucatu. 119p.
(Doctoral Thesis. Universidade Estadual Paulista - UNESP). Available at: <http://www.ibb.unesp.
br/posgrad/teses/zoologia_do_2007_rodrigo_almeida.pdf> Access on: 20 Nov. 2014.
DE BEM, J.C. 2009 Desenvolvimento gonadal inicial e reversão sexual em Astyanax altiparanae (Teleostei,Characidae). Rio Claro. 96p. (Masters Dissertation.Universidade Estadual Paulista - UNESP).Available at: <http://repositorio.unesp.br/bitstream/handle/11449/87742/bem_jc_me_rcl
a.pdf?sequence=1&isAllowed=y> Access on: 20 Nov. 2014.
DE ROOIJ, D.G. and RUSSELL, L.D. 2000 All you wanted to know about spermatogonia but were
afraid to ask. Journal of Andrology, 21(6): 776-798.
GARUTTI, V. and BRITSKI, H.A. 2000 Descrição de uma espécie nova de Astyanax (Teleostei:
Characidae) da bacia do alto Rio Paraná e considerações gerais sobre as demais espécies do
gênero na bacia. Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, 13:
65-88.
GRIER, H.J.; LINTON, J.R.; LEATHERLAND, J.F.; VLAMING, V.L. 1980 Structural evidence for
two different testicular types in Teleost fishes. The American Journal of Anatomy, 159(3): 331-345.
GRIER, H.J. and ARANZÁBAL, M.C.U. 2009 The testis and spermatogenesis in Teleosts. In:
JAMIESON, B.G.M. Reproductive Biology and Phylogeny of Fishes: Agnathans and Bony Fishes, 8.
St. Lucia: University of Queensland Press.p.119-142.
QUAGIO-GRASSIOTTO, I.; GAMIERO, M.C.;SCHNEIDER, T.; MALABARBA, L.R.; OLIVEIRA,C. 2003 Spermiogenesis and spermatozoa ultrastructure in five species of the Curimatidae with some considerations of spermatozoa ultrastructure in the Characiformes. Neotropical Ichthyology, 1(1): 35-45
JAMIESON, B.G.M. 1991 Fish Evolution and Systematics: Evidence from spermatozoa.
Cambridge: Cambridge University Press. 319p.
LEAL, M.C.; CARDOSO, E.R.; NOBREGA, R.H.;BATLOUNI, S.R.; BOGERD, J.; FRANí"¡A, L.R.; SCHULZ, R.W. 2009 Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biology of Reproduction, 81(1): 77-187.
LO NOSTRO, F.; GRIER, H.; GUERRERO, G.A. 2003 Involvement of the gonadal germinal epithelium
during sex reversal and seasonal testicular cycling in the protogynous swamp eel,Synbranchus marmoratus Bloch 1795 (Teleostei,Synbranchidae). Journal of Morphology, 257(1):107-126.
LOPES, D.C.J.R.; BAZZOLI, N.; BRITO, M.F.G.;MARIA, T.A. 2004 Male reproductive apparatus
in the South American catfish Conorhynchus conirostris. Journal of Fish Biology, 64(5): 1419-1424.
MAZZOLDI, C.; LORENZI, V.; RASOTTO, M.B. 2007 Variation of male reproductive apparatus in
relation to fertilization modalities in the catfish families Auchenipteridae and Callichthyidae
(Teleostei: Siluriformes). Journal of Fish Biology,70(1): 243-256.
MORENA, A.R.; BOITANI, C.; PESCE, M.; FELICI,M.; STEFANINI M. 1996 Isolation of Highly
Purified Type A Spermatogonia From Prepubertal Rat Testis. Journal of Andrology,17(6): 708-717.
NÓBREGA, R.H.; LO NOSTRO, F.L.; GRIER, HARRY, J.; QUAGIO-GRASSIOTTO, I. 2006 Cellular proliferation in fish male germinal epithelium. In: INTERNATIONAL SYMPOSIUM ON ANIMAL BIOLOGY OF REPRODUCTION -From sex differentiation to reproductive biotechnology. Animal Reproduction, 3: 199-199.
NÓBREGA, R.H.; LACERDA, S.M.N.S.; COSTA, G.M.J.; SILVA, R.C.; SCHULZ, R.W.; FRANí"¡A,
L.R. 2008 Development of germ cell transplantation in zebrafish (Danio rerio): a means to study the spermatogonial stem cells in fish. In: INTERNATIONAL SYMPOSIUM ON ANIMAL BIOLOGY OF REPRODUCTION, 2.,São Paulo, 19-22/Nov./2008. Anais… São Paulo:Brazilian College of Animal Reproduction.
NÓBREGA, R.H.; BATLOUNI, S.R.; FRANí"¡A, L.R.2009 An overview of functional and stereological
evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiology
Biochemistry, 35(1): 197-206.
NÓBREGA, R.H.; GREEBE, C.; DE KANT, H.V.; BOGERD J.; FRANí"¡A, L.R.; SCHULZ, R.W. 2010 Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PlosOne, 5(9): e12808. [on line] doi:10.1371/journal.pone.0012808
ORSI, M.L.; SHIBATTA, O.A.; SILVA-SOUZA, A.T.2002 Caracterização biológica de populações de
peixes do rio Tibagi, localidade de Sertanópolis. In: MEDRI, M.E.; BIANCHINI, E.; SHIBATTA,
O.A.; PIMENTA, J.A. A bacia do rio Tibagi. Londrina: Universidade Estadual de Londrina.
p.425-432.
REIS, R.E.; KULLANDER, S.O.; FERRARIS JR, C.J. 2003 Check list of the freshwater fishes of South and
Central America. Porto Alegre: PUCRS Press. 742p.
ROOSE-RUNGE, E.C. 1962 The process of spermatogenesis in mammals. Biological Reviews,
37(3): 343-377.
RUSSELL, L.D.; ETTLIN, R.A.; SINHA HIKIM, A.P.;CLEGG, E.D. 1990 Mammalian spermatogenesis.
Histological and histopathological evaluation of the testis. Clearwater: Cache River Press. 40p.
SCHULZ, R.W.; MENTING, S.; BOGERD, J.;FRANí"¡A, L.R.; VILELA, D.A.R; GODINHO, H.P. 2005 Sertoli cell proliferation in the adult testis: evidence from two fish species belonging to different orders. Biology of Reproduction, 73(5):891-898.
SCHULZ, R.W.; FRANí"¡A, L.R.; LAREYRE, J.J.;LEGAC, F.; CHIARINI-GARCIA, H.; NOBREGA, R.H.; MIURA, T. 2010 Spermatogenesis in fish. General and Comparative Endocrinology, 165(3): 390-411.
SILVA, M. 1987 Morfologia ultra-estrutural do testículo,cinética da espermatogênese e barreira hemotesticular da tilápia do Nilo, Oreochromis niloticus. Belo Horizonte. 164p. (Doctoral Thesis. Universidade Federal de Minas Gerais - UFMG).
SIQUEIRA-SILVA, D.H.; DA-SILVA-COSTA, R.; NINHAUS-SILVEIRA, A.; VICENTINI, C.A.;VERÍSSIMO-SILVEIRA, R. 2012 Ultrastructural analysis of spermiogenesis in the neotropical cichlid Kullander & Ferreira, 2006 (Perciformes:Cichlidae). Journal of Applied Ichthyology, 28(6):878-882.
SIQUEIRA-SILVA, D.H.D.; VICENTINI, C.A.;NINHAUS-SILVEIRA, A.; VERISSIMO-SILVEIRA, R. 2013 Reproductive cycle of the Neotropical cichlid yellow peacock bass Cichla kelberi: A novel pattern of testicular development. Neotropical Ichthyology, 11(3): 587-596.
VAZZOLER, A.E.A.M. 1996 Biologia da reprodução de peixes teleósteos: teoria e prática. Maringá: Eduem. 169p.
VERÍSSIMO-SILVEIRA, R.; GUSMÃO-POMPIANI,P.; VICENTINI, C.A.; QUAGIO-GRASSIOTTO,I. 2006 Spermiogenesis and spermatozoa ultrastructure in Salminus and Brycon, two primitive genera in Characidae (Teleostei:Ostariophysi: Characiformes). Acta Zoologica,87(4): 305-313.
VILELA, D.A.R.; SILVA, S.G.B.; PEIXOTO, M.T.D.;GODINHO, H.P.; FRANí"¡A, L.R. 2003 Spermatogenesis in teleost: insights from the Nile tilapia (Oreochromis niloticus) model. Fish
Physiology and Biochemistry, 28(1): 187-190.
VERGÍLIO, C.S.; MOREIRA, R.V.; CARVALHO,C.E.V.; MELO, E.J.T. 2012 Characterization of
mature testis and sperm morphology of Gymnotus carapo (Gymnotidae, Teleostei) from
the southeast of Brazil. Acta Zoologica, 0: 1-7.
YASUI, G.S.; SANTOS, M.P.; NAKAGHI, L.S.O.;SENHORINI, J.A.; ARIAS-RODRIGUEZ, L.; FUJIMOTO, T.; SHIMODA, E.; SILVA, L.A. 2014 Improvement of gamete quality and its shortterm storage: an approach for biotechnology in laboratory fish. Animal, 9(3): 464-470.
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2018-11-20
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