New directions in assisted breeding techniques for fish conservation
Nicola Rivers A D , Jonathan Daly B C and Peter Temple-Smith AA Department of Obstetrics and Gynaecology, School of Clinical Sciences, Monash University, Melbourne, Vic. 3168, Australia.
B Smithsonian Conservation Biology Institute, Front Royal, VA 22360, USA.
C Hawaii Institute of Marine Biology, 46-007 Lilipuna Road, Kaneohe, HI 96744, USA.
D Corresponding author. Email: nicola.rivers@monash.edu
Reproduction, Fertility and Development 32(9) 807-821 https://doi.org/10.1071/RD19457
Submitted: 13 December 2019 Accepted: 26 April 2020 Published: 2 June 2020
Journal Compilation © CSIRO 2020 Open Access CC BY
Abstract
Fish populations continue to decline globally, signalling the need for new initiatives to conserve endangered species. Over the past two decades, with advances in our understanding of fish germ line biology, new ex situ management strategies for fish genetics and reproduction have focused on the use of germ line cells. The development of germ cell transplantation techniques for the purposes of propagating fish species, most commonly farmed species such as salmonids, has been gaining interest among conservation scientists as a means of regenerating endangered species. Previously, ex situ conservation methods in fish have been restricted to the cryopreservation of gametes or maintaining captive breeding colonies, both of which face significant challenges that have restricted their widespread implementation. However, advances in germ cell transplantation techniques have made its application in endangered species tangible. Using this approach, it is possible to preserve the genetics of fish species at any stage in their reproductive cycle regardless of sexual maturity or the limitations of brief annual spawning periods. Combining cryopreservation and germ cell transplantation will greatly expand our ability to preserve functional genetic samples from threatened species, to secure fish biodiversity and to produce new individuals to enhance or restore native populations.
Additional keywords: cryoconservation, gonad cryopreservation, cryopreservation, germ cell transplantation, fish biology, sterilisation.
References
Bellaiche, J., Lareyre, J. J., Cauty, C., Yano, A., Allemand, I., and Le Gac, F. (2014). Spermatogonial stem cell quest: nanos2, marker of a subpopulation of undifferentiated A spermatogonia in trout testis. Biol. Reprod. 90, 79.| Spermatogonial stem cell quest: nanos2, marker of a subpopulation of undifferentiated A spermatogonia in trout testis.Crossref | GoogleScholarGoogle Scholar | 24554733PubMed |
Benfey, T. J., and Sutterlin, A. M. (1984). Triploidy induced by heat shock and hydrostatic pressure in landlocked Atlantic salmon (Salmo salar L.). Aquaculture 36, 359–367.
| Triploidy induced by heat shock and hydrostatic pressure in landlocked Atlantic salmon (Salmo salar L.).Crossref | GoogleScholarGoogle Scholar |
Blaser, H., Reichman-Fried, M., Castanon, I., Dumstrei, K., Marlow, F. L., Kawakami, K., Solnica-Krezel, L., Heisenberg, C. P., and Raz, E. (2006). Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev. Cell 11, 613–627.
| Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow.Crossref | GoogleScholarGoogle Scholar | 17084355PubMed |
Blomqvist, D., Pauliny, A., Larsson, M., and Flodin, L.-A. (2010). Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population. BMC Evol. Biol. 10, 33.
| Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population.Crossref | GoogleScholarGoogle Scholar | 20122269PubMed |
Braat, A. K., Zandbergen, T., Van De Water, S., Goos, H. J., and Zivkovic, D. (1999). Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA. Dev. Dyn. 216, 153–167.
| Characterization of zebrafish primordial germ cells: morphology and early distribution of vasa RNA.Crossref | GoogleScholarGoogle Scholar | 10536055PubMed |
Cassani, J. R., and Caton, W. E. (1986). Efficient production of triploid grass carp (Ctenopharyngodon idella) utilizing hydrostatic pressure. Aquaculture 55, 43–50.
| Efficient production of triploid grass carp (Ctenopharyngodon idella) utilizing hydrostatic pressure.Crossref | GoogleScholarGoogle Scholar |
Chilmonczyk, S. (1992). The thymus in fish: development and possible function in the immune response. Annu. Rev. Fish Dis. 2, 181–200.
| The thymus in fish: development and possible function in the immune response.Crossref | GoogleScholarGoogle Scholar |
Chourrout, D. (1984). Pressure-induced retention of second polar body and suppression of first cleavage in rainbow trout: production of all-triploids, all-tetraploids, and heterozygous and homozygous diploid gynogenetics. Aquaculture 36, 111–126.
| Pressure-induced retention of second polar body and suppression of first cleavage in rainbow trout: production of all-triploids, all-tetraploids, and heterozygous and homozygous diploid gynogenetics.Crossref | GoogleScholarGoogle Scholar |
Clarke, A. G. (2009). The Frozen Ark Project: the role of zoos and aquariums in preserving the genetic material of threatened animals. Int. Zoo Yearb. 43, 222–230.
| The Frozen Ark Project: the role of zoos and aquariums in preserving the genetic material of threatened animals.Crossref | GoogleScholarGoogle Scholar |
Clelland, E., and Peng, C. (2009). Endocrine/paracrine control of zebrafish ovarian development. Mol. Cell. Endocrinol. 312, 42–52.
| Endocrine/paracrine control of zebrafish ovarian development.Crossref | GoogleScholarGoogle Scholar | 19406202PubMed |
Couture, R., Schamber, T., Firmenich, A., and Banner, C. (2007). Pressure shock induction of triploid rainbow trout. (Oregon Department of Fish and Wildlife Oregon: Corvallis.) Available at https://www.dfw.state.or.us/fish/OHRC/docs/2013/pubs/Pressure_Shock_Induction_of_Triploid_Rainbow_Trout.pdf [verified 21 May 2020].
Dai, X., Jin, X., Chen, X., He, J., and Yin, Z. (2015). Sufficient numbers of early germ cells are essential for female sex development in zebrafish. PLoS One 10, e0117824.
| Sufficient numbers of early germ cells are essential for female sex development in zebrafish.Crossref | GoogleScholarGoogle Scholar | 26660527PubMed |
Daly, J., Galloway, D., Bravington, W., Holland, M., and Ingram, B. (2008). Cryopreservation of sperm from Murray cod, Maccullochella peelii peelii. Aquaculture 285, 117–122.
| Cryopreservation of sperm from Murray cod, Maccullochella peelii peelii.Crossref | GoogleScholarGoogle Scholar |
de Siqueira-Silva, D. H., dos Santos Silva, A. P., Ninhaus-Silveira, A., and Veríssimo-Silveira, R. (2015). The effects of temperature and busulfan (Myleran) on the yellowtail tetra Astyanax altiparanae (Pisces, Characiformes) spermatogenesis. Theriogenology 84, 1033–1042.
| The effects of temperature and busulfan (Myleran) on the yellowtail tetra Astyanax altiparanae (Pisces, Characiformes) spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 26164805PubMed |
de Siqueira-Silva, D. H., Saito, T., Dos Santos-Silva, A. P., da Silva Costa, R., Psenicka, M., and Yasui, G. S. (2018). Biotechnology applied to fish reproduction: tools for conservation. Fish Physiol. Biochem. 44, 1469–1485.
| Biotechnology applied to fish reproduction: tools for conservation.Crossref | GoogleScholarGoogle Scholar | 29707740PubMed |
Don, J., and Avtalion, R. R. (1986). The induction of triploidy in Oreochromis aureus by heat shock. Theor. Appl. Genet. 72, 186–192.
| The induction of triploidy in Oreochromis aureus by heat shock.Crossref | GoogleScholarGoogle Scholar | 24247833PubMed |
Dranow, D. B., Tucker, R. P., and Draper, B. W. (2013). Germ cells are required to maintain a stable sexual phenotype in adult zebrafish. Dev. Biol. 376, 43–50.
| Germ cells are required to maintain a stable sexual phenotype in adult zebrafish.Crossref | GoogleScholarGoogle Scholar | 23348677PubMed |
Edgar, G. J., Ward, T. J., and Stuart-Smith, R. D. (2018). Rapid declines across Australian fishery stocks indicate global sustainability targets will not be achieved without an expanded network of ‘no-fishing’ reserves. Aquat. Conserv. 28, 1337–1350.
| Rapid declines across Australian fishery stocks indicate global sustainability targets will not be achieved without an expanded network of ‘no-fishing’ reserves.Crossref | GoogleScholarGoogle Scholar |
Eno, C., and Pelegri, F. (2016). Germ cell determinant transmission, segregation, and function in the zebrafish embryo. In ‘Insights from Animal Reproduction’. (Ed. R. Payan-Carreira.) pp. 115–142. (InTech: Rijeka, Croatia.)
Extavour, C. G., and Akam, M. (2003). Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869–5884.
| Mechanisms of germ cell specification across the metazoans: epigenesis and preformation.Crossref | GoogleScholarGoogle Scholar | 14597570PubMed |
Farlora, R., Hattori-Ihara, S., Takeuchi, Y., Hayashi, M., Octavera, A., Alimuddin, , and Yoshizaki, G. (2014). Intraperitoneal germ cell transplantation in the Nile tilapia Oreochromis niloticus. Mar. Biotechnol. (NY) 16, 309–320.
| Intraperitoneal germ cell transplantation in the Nile tilapia Oreochromis niloticus.Crossref | GoogleScholarGoogle Scholar | 24096828PubMed |
Figueroa, E., Merino, O., Risopatrón, J., Isachenko, V., Sánchez, R., Effer, B., Isachenko, E., Farias, J. G., and Valdebenito, I. (2015). Effect of seminal plasma on Atlantic salmon (Salmo salar) sperm vitrification. Theriogenology 83, 238–245.e2.
| Effect of seminal plasma on Atlantic salmon (Salmo salar) sperm vitrification.Crossref | GoogleScholarGoogle Scholar | 25442390PubMed |
Franěk, R., Marinovic, Z., Lujic, J., Urbanyi, B., Fucikova, M., Kaspar, V., Psenicka, M., and Horvath, A. (2019). Cryopreservation and transplantation of common carp spermatogonia. PLoS One 14, e0205481.
| Cryopreservation and transplantation of common carp spermatogonia.Crossref | GoogleScholarGoogle Scholar | 30998742PubMed |
Fujimoto, T., Nishimura, T., Goto-Kazeto, R., Kawakami, Y., Yamaha, E., and Arai, K. (2010). Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish. Proc. Natl Acad. Sci. USA 107, 17211–17216.
| Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish.Crossref | GoogleScholarGoogle Scholar | 20855617PubMed |
Golpour, A., Siddique, M. A. M., Rodina, M., and Pšenička, M. (2016). Short-term storage of sterlet Acipenser ruthenus testicular cells at –80 °C. Cryobiology 72, 154–156.
| Short-term storage of sterlet Acipenser ruthenus testicular cells at –80 °C.Crossref | GoogleScholarGoogle Scholar | 26964775PubMed |
Goto, R., and Saito, T. (2019). A state-of-the-art review of surrogate propagation in fish. Theriogenology 133, 216–227.
| A state-of-the-art review of surrogate propagation in fish.Crossref | GoogleScholarGoogle Scholar | 31155037PubMed |
Goto, R., Saito, T., Takeda, T., Fujimoto, T., Takagi, M., Arai, K., and Yamaha, E. (2012). Germ cells are not the primary factor for sexual fate determination in goldfish. Dev. Biol. 370, 98–109.
| Germ cells are not the primary factor for sexual fate determination in goldfish.Crossref | GoogleScholarGoogle Scholar | 22824426PubMed |
Goto, R., Saito, T., Kawakami, Y., Kitauchi, T., Takagi, M., Todo, T., Arai, K., and Yamaha, E. (2015). Visualization of primordial germ cells in the fertilized pelagic eggs of the barfin flounder Verasper moseri. Int. J. Dev. Biol. 59, 465–470.
| Visualization of primordial germ cells in the fertilized pelagic eggs of the barfin flounder Verasper moseri.Crossref | GoogleScholarGoogle Scholar | 26864487PubMed |
Hagedorn, M., Hsu, E., Kleinhans, F. W., and Wildt, D. E. (1997). New approaches for studying the permeability of fish embryos: toward successful cryopreservation. Cryobiology 34, 335–347.
| New approaches for studying the permeability of fish embryos: toward successful cryopreservation.Crossref | GoogleScholarGoogle Scholar | 9200820PubMed |
Hagedorn, M. M., Daly, J. P., Carter, V. L., Cole, K. S., Jaafar, Z., Lager, C. V. A., and Parenti, L. R. (2018). Cryopreservation of fish spermatogonial cells: the future of natural history collections. Sci. Rep. 8, 6149.
| Cryopreservation of fish spermatogonial cells: the future of natural history collections.Crossref | GoogleScholarGoogle Scholar | 29670253PubMed |
Hamasaki, M., Takeuchi, Y., Yazawa, R., Yoshikawa, S., Kadomura, K., Yamada, T., Miyaki, K., Kikuchi, K., and Yoshizaki, G. (2017). Production of tiger puffer Takifugu rubripes offspring from triploid grass puffer Takifugu niphobles parents. Mar. Biotechnol. (NY) 19, 579–591.
| Production of tiger puffer Takifugu rubripes offspring from triploid grass puffer Takifugu niphobles parents.Crossref | GoogleScholarGoogle Scholar | 28942506PubMed |
Hammed, A. M., Fashina-Bombata, H. A., and Osinaike, A. O. (2010). The use of cold shock in inducing triploidy in African mud catfish (Clarias gariepinus). Afr. J. Biotechnol. 9, 1844–1847.
| The use of cold shock in inducing triploidy in African mud catfish (Clarias gariepinus).Crossref | GoogleScholarGoogle Scholar |
Hartung, O., and Marlow, F. L. (2014). Get it together: how RNA-binding proteins assemble and regulate germ plasm in the oocyte and embryo. In ‘Zebrafish: Topics in Reproduction, Toxicology and Development’. (Eds C. A. Lessman and E. A. Carver.) pp. 65–106. (Nova Science Publishers, Inc.: New York, USA.)
Hartung, O., Forbes, M. M., and Marlow, F. L. (2014). Zebrafish vasa is required for germ-cell differentiation and maintenance. Mol. Reprod. Dev. 81, 946–961.
| Zebrafish vasa is required for germ-cell differentiation and maintenance.Crossref | GoogleScholarGoogle Scholar | 25257909PubMed |
Higaki, S., Eto, Y., Kawakami, Y., Yamaha, E., Kagawa, N., Kuwayama, M., Nagano, M., Katagiri, S., and Takahashi, Y. (2010). Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos. Reproduction 139, 733–740.
| Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos.Crossref | GoogleScholarGoogle Scholar | 20154175PubMed |
Higaki, S., Kawakami, Y., Eto, Y., Yamaha, E., Nagano, M., Katagiri, S., Takada, T., and Takahashi, Y. (2013). Cryopreservation of zebrafish (Danio rerio) primordial germ cells by vitrification of yolk-intact and yolk-depleted embryos using various cryoprotectant solutions. Cryobiology 67, 374–382.
| Cryopreservation of zebrafish (Danio rerio) primordial germ cells by vitrification of yolk-intact and yolk-depleted embryos using various cryoprotectant solutions.Crossref | GoogleScholarGoogle Scholar | 24383132PubMed |
Higaki, S., Shimada, M., Kawamoto, K., Todo, T., Kawasaki, T., Tooyama, I., Fujioka, Y., Sakai, N., and Takada, T. (2017). In vitro differentiation of fertile sperm from cryopreserved spermatogonia of the endangered endemic cyprinid honmoroko (Gnathopogon caerulescens). Sci. Rep. 7, 42852.
| In vitro differentiation of fertile sperm from cryopreserved spermatogonia of the endangered endemic cyprinid honmoroko (Gnathopogon caerulescens).Crossref | GoogleScholarGoogle Scholar | 28211534PubMed |
Huergo, G. M., and Zaniboni-Filho, E. (2006). Triploidy induction in Jundiá, Rhamdia quelen, through hydrostatic pressure shock. J. Appl. Aquacult. 18, 45–57.
| Triploidy induction in Jundiá, Rhamdia quelen, through hydrostatic pressure shock.Crossref | GoogleScholarGoogle Scholar |
Ichida, K., Kise, K., Morita, T., Yazawa, R., Takeuchi, Y., and Yoshizaki, G. (2017). Flow-cytometric enrichment of Pacific bluefin tuna type A spermatogonia based on light-scattering properties. Theriogenology 101, 91–98.
| Flow-cytometric enrichment of Pacific bluefin tuna type A spermatogonia based on light-scattering properties.Crossref | GoogleScholarGoogle Scholar | 28708521PubMed |
Cresswell, I. D., and Murphy, H. (2016). Biodiversity: Freshwater species and ecosystems. In ‘Australia State of the Environment 2016.’ (Australian Government Department of the Environment and Energy: Canberra.)
Janik, M., Kleinhans, F. W., and Hagedorn, M. (2000). Overcoming a permeability barrier by microinjecting cryoprotectants into zebrafish embryos (Brachydanio rerio). Cryobiology 41, 25–34.
| Overcoming a permeability barrier by microinjecting cryoprotectants into zebrafish embryos (Brachydanio rerio).Crossref | GoogleScholarGoogle Scholar | 11017758PubMed |
Khosla, K., Wang, Y., Hagedorn, M., Qin, Z., and Bischof, J. (2017). Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano 11, 7869–7878.
| Gold nanorod induced warming of embryos from the cryogenic state enhances viability.Crossref | GoogleScholarGoogle Scholar | 28702993PubMed |
Kise, K., Yoshikawa, H., Sato, M., Tashiro, M., Yazawa, R., Nagasaka, Y., Takeuchi, Y., and Yoshizaki, G. (2012). Flow-cytometric isolation and enrichment of teleost type A spermatogonia based on light-scattering properties. Biol. Reprod. 86, 107.
| Flow-cytometric isolation and enrichment of teleost type A spermatogonia based on light-scattering properties.Crossref | GoogleScholarGoogle Scholar | 22219211PubMed |
Kobayashi, T., Takeuchi, Y., Yoshizaki, G., and Takeuchi, T. (2003). Cryopreservation of trout primordial germ cells. Fish Physiol. Biochem. 28, 479–480.
| Cryopreservation of trout primordial germ cells.Crossref | GoogleScholarGoogle Scholar |
Kobayashi, T., Yoshizaki, G., Takeuchi, Y., and Takeuchi, T. (2004). Isolation of highly pure and viable primordial germ cells from rainbow trout by GFP-dependent flow cytometry. Mol. Reprod. Dev. 67, 91–100.
| Isolation of highly pure and viable primordial germ cells from rainbow trout by GFP-dependent flow cytometry.Crossref | GoogleScholarGoogle Scholar | 14648879PubMed |
Kobayashi, T., Takeuchi, Y., Takeuchi, T., and Yoshizaki, G. (2007). Generation of viable fish from cryopreserved primordial germ cells. Mol. Reprod. Dev. 74, 207–213.
| Generation of viable fish from cryopreserved primordial germ cells.Crossref | GoogleScholarGoogle Scholar | 16998845PubMed |
Köprunner, M., Thisse, C., Thisse, B., and Raz, E. (2001). A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev. 15, 2877–2885.
| 11691838PubMed |
Lacerda, S. M. S. N., Batlouni, S. R., Costa, J. M. G., Segatelli, T. M., Quirino, B. R., Queiroz, B. M., Kalapothakis, E., and Franca, L. R. (2010). A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model. PLoS One 5, e10740.
| A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model.Crossref | GoogleScholarGoogle Scholar |
Lacerda, S. M. S. N., Costa, G. M. J., and de França, L. R. (2014). Biology and identity of fish spermatogonial stem cell. Gen. Comp. Endocrinol. 207, 56–65.
| Biology and identity of fish spermatogonial stem cell.Crossref | GoogleScholarGoogle Scholar |
Lee, S., and Yoshizaki, G. (2016). Successful cryopreservation of spermatogonia in critically endangered Manchurian trout (Brachymystax lenok). Cryobiology 72, 165–168.
| Successful cryopreservation of spermatogonia in critically endangered Manchurian trout (Brachymystax lenok).Crossref | GoogleScholarGoogle Scholar | 26827783PubMed |
Lee, S., Iwasaki, Y., Shikina, S., and Yoshizaki, G. (2013). Generation of functional eggs and sperm from cryopreserved whole testes. Proc. Natl Acad. Sci. USA 110, 1640–1645.
| Generation of functional eggs and sperm from cryopreserved whole testes.Crossref | GoogleScholarGoogle Scholar | 23319620PubMed |
Lee, S., Seki, S., Katayama, N., and Yoshizaki, G. (2015). Production of viable trout offspring derived from frozen whole fish. Sci. Rep. 5, 16045.
| Production of viable trout offspring derived from frozen whole fish.Crossref | GoogleScholarGoogle Scholar | 26522018PubMed |
Lee, S., Katayama, N., and Yoshizaki, G. (2016). Generation of juvenile rainbow trout derived from cryopreserved whole ovaries by intraperitoneal transplantation of ovarian germ cells. Biochem. Biophys. Res. Commun. 478, 1478–1483.
| Generation of juvenile rainbow trout derived from cryopreserved whole ovaries by intraperitoneal transplantation of ovarian germ cells.Crossref | GoogleScholarGoogle Scholar | 27581197PubMed |
Li, M., Hong, N., Xu, H., Song, J., and Hong, Y. (2016). Germline replacement by blastula cell transplantation in the fish medaka. Sci. Rep. 6, 29658.
| Germline replacement by blastula cell transplantation in the fish medaka.Crossref | GoogleScholarGoogle Scholar | 27406328PubMed |
Linhartová, Z., Rodina, M., Guralp, H., Gazo, I., Saito, T., and Pšenička, M. (2014). Isolation and cryopreservation of early stages of germ cells of tench (Tinca tinca). Czech J. Anim. Sci. 59, 381–390.
| Isolation and cryopreservation of early stages of germ cells of tench (Tinca tinca).Crossref | GoogleScholarGoogle Scholar |
Lintermans, M. (2007). ‘Fishes of the Murray–Darling Basin: An Introductory Guide.’ (Murray-Darling Basin Authority: Canberra, Australia)
Lubzens, E., Young, G., Bobe, J., and Cerdà, J. (2010). Oogenesis in teleosts: how fish eggs are formed. Gen. Comp. Endocrinol. 165, 367–389.
| Oogenesis in teleosts: how fish eggs are formed.Crossref | GoogleScholarGoogle Scholar | 19505465PubMed |
Lujić, J., Marinović, Z., Sušnik Bajec, S., Djurdjevič, I., Kása, E., Urbányi, B., and Horváth, Á. (2017). First successful vitrification of salmonid ovarian tissue. Cryobiology 76, 154–157.
| First successful vitrification of salmonid ovarian tissue.Crossref | GoogleScholarGoogle Scholar | 28438562PubMed |
Majhi, S. K., Hattori, R. S., Yokota, M., Watanabe, S., and Strüssmann, C. A. (2009). Germ cell transplantation using sexually competent fish: an approach for rapid propagation of endangered and valuable germlines. PLoS One 4, e6132.
| Germ cell transplantation using sexually competent fish: an approach for rapid propagation of endangered and valuable germlines.Crossref | GoogleScholarGoogle Scholar | 19572014PubMed |
Majhi, S. K., Hattori, R. S., Rahman, S. M., and Strussmann, C. A. (2014). Surrogate production of eggs and sperm by intrapapillary transplantation of germ cells in cytoablated adult fish. PLoS One 9, e95294.
| Surrogate production of eggs and sperm by intrapapillary transplantation of germ cells in cytoablated adult fish.Crossref | GoogleScholarGoogle Scholar | 24748387PubMed |
Malison, J. A., Procarione, L. S., Held, J. A., Kayes, T. B., and Amundson, C. H. (1993). The influence of triploidy and heat and hydrostatic pressure shocks on the growth and reproductive development of juvenile yellow perch (Perca jlavescens). Aquaculture 116, 121–133.
| The influence of triploidy and heat and hydrostatic pressure shocks on the growth and reproductive development of juvenile yellow perch (Perca jlavescens).Crossref | GoogleScholarGoogle Scholar |
Matsuda, M. (2003). Sex determination in fish: lessons from the sex-determining gene of the teleost medaka, Oryzias latipes. Dev. Growth Differ. 45, 397–403.
| Sex determination in fish: lessons from the sex-determining gene of the teleost medaka, Oryzias latipes.Crossref | GoogleScholarGoogle Scholar | 14706065PubMed |
McMillan, D. B. (2007). ‘Fish Histology Female Reproductive Systems.’ (Springer Verlag: Dordrecht.)
Murray–Darling Basin Authority (MDBA) (2019). Response to recent fish deaths: recommended action plan. Available at https://www.mdba.gov.au/sites/default/files/pubs/Response-fish-death-events-recommended-action%20plan-2019_0.pdf [verified 21 May 2020].
Nishimura, T., and Tanaka, M. (2014). Gonadal development in fish. Sex Dev. 8, 252–261.
| Gonadal development in fish.Crossref | GoogleScholarGoogle Scholar | 25034975PubMed |
Nynca, J., Dietrich, G. J., Dobosz, S., Grudniewska, J., and Ciereszko, A. (2014). Effect of cryopreservation on sperm motility parameters and fertilizing ability of brown trout semen. Aquaculture 433, 62–65.
| Effect of cryopreservation on sperm motility parameters and fertilizing ability of brown trout semen.Crossref | GoogleScholarGoogle Scholar |
Okutsu, T., Suzuki, K., Takeuchi, Y., Takeuchi, T., and Yoshizaki, G. (2006a). Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc. Natl Acad. Sci. USA 103, 2725–2729.
| Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish.Crossref | GoogleScholarGoogle Scholar | 16473947PubMed |
Okutsu, T., Yano, A., Nagasawa, K., Shikina, S., Kobayashi, T., Takeuchi, Y., and Yoshizaki, G. (2006b). Manipulation of fish germ cell: visualization, cryopreservation and transplantation. J. Reprod. Dev. 52, 685–693.
| Manipulation of fish germ cell: visualization, cryopreservation and transplantation.Crossref | GoogleScholarGoogle Scholar | 17220596PubMed |
Okutsu, T., Shikina, S., Kanno, M., Takeuchi, Y., and Yoshizaki, G. (2007). Production of trout offspring from triploid salmon parents. Science 317, 1517.
| Production of trout offspring from triploid salmon parents.Crossref | GoogleScholarGoogle Scholar | 17872437PubMed |
Otake, H., Shinomiya, A., Matsuda, M., Hamaguchi, S., and Sakaizumi, M. (2006). Wild-derived XY sex-reversal mutants in the medaka, Oryzias latipes. Genetics 173, 2083–2090.
| Wild-derived XY sex-reversal mutants in the medaka, Oryzias latipes.Crossref | GoogleScholarGoogle Scholar | 16702419PubMed |
Pandian, T. J., and Kirankumar, S. (2003). Androgenesis and conservation of fishes. Curr. Sci. 85, 917–931.
Papah, M. B., Kisia, S. M., Ojoo, R. O., Makanya, A. N., Wood, C. M., Kavembe, G. D., Maina, J. N., Johannsson, O. E., Bergman, H. L., Laurent, P., Chevalier, C., Bianchini, A., Bianchini, L. F., and Onyango, D. W. (2013). Morphological evaluation of spermatogenesis in Lake Magadi tilapia (Alcolapia grahami): a fish living on the edge. Tissue Cell 45, 371–382.
| Morphological evaluation of spermatogenesis in Lake Magadi tilapia (Alcolapia grahami): a fish living on the edge.Crossref | GoogleScholarGoogle Scholar | 23916093PubMed |
Pearson, P. L. (2001). Triploidy. In ‘Encyclopedia of Genetics’. (Eds S. Brenner and J. H. Miller.) pp. 2055–2056. (Academic Press: New York.)
Peruzzi, S., and Chatain, B. (2000). Pressure and cold shock induction of meiotic gynogenesis and triploidy in the European sea bass, Dicentrarchus labrax L.: relative efficiency of methods and parental variability. Aquaculture 189, 23–37.
| Pressure and cold shock induction of meiotic gynogenesis and triploidy in the European sea bass, Dicentrarchus labrax L.: relative efficiency of methods and parental variability.Crossref | GoogleScholarGoogle Scholar |
Peruzzi, S., Kettunen, A., Primicerio, R., and Kaurić, G. (2007). Thermal shock induction of triploidy in Atlantic cod (Gadus morhua L.). Aquacult. Res. 38, 926–932.
| Thermal shock induction of triploidy in Atlantic cod (Gadus morhua L.).Crossref | GoogleScholarGoogle Scholar |
Pradeep, P. J., Srijaya, T. C., Hassan, A., Chatterji, A. K., Withyachumnarnkul, B., and Jeffs, A. (2014). Optimal conditions for cold-shock induction of triploidy in red tilapia. Aquacult. Int. 22, 1163–1174.
Pšenička, M., Saito, T., Linhartová, Z., and Gazo, I. (2015). Isolation and transplantation of sturgeon early-stage germ cells. Theriogenology 83, 1085–1092.
| Isolation and transplantation of sturgeon early-stage germ cells.Crossref | GoogleScholarGoogle Scholar | 25559841PubMed |
Raz, E., and Reichman-Fried, M. (2006). Attraction rules: germ cell migration in zebrafish. Curr. Opin. Genet. Dev. 16, 355–359.
| Attraction rules: germ cell migration in zebrafish.Crossref | GoogleScholarGoogle Scholar | 16806897PubMed |
Riesco, M. F., Martinez-Pastor, F., Chereguini, O., and Robles, V. (2012). Evaluation of zebrafish (Danio rerio) PGCs viability and DNA damage using different cryopreservation protocols. Theriogenology 77, 122–130.e2.
| Evaluation of zebrafish (Danio rerio) PGCs viability and DNA damage using different cryopreservation protocols.Crossref | GoogleScholarGoogle Scholar | 21872308PubMed |
Saito, T., Fujimoto, T., Maegawa, S., Inoue, K., Tanaka, M., Arai, K., and Yamaha, E. (2006). Visualization of primordial germ cells in vivo using GFP-nos1 3′UTR mRNA. Int. J. Dev. Biol. 50, 691–699.
| Visualization of primordial germ cells in vivo using GFP-nos1 3′UTR mRNA.Crossref | GoogleScholarGoogle Scholar | 17051479PubMed |
Saito, T., Goto-Kazeto, R., Arai, K., and Yamaha, E. (2008). Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol. Reprod. 78, 159–166.
| Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation.Crossref | GoogleScholarGoogle Scholar | 17901077PubMed |
Saito, T., Goto-Kazeto, R., Fujimoto, T., Kawakami, Y., Arai, K., and Yamaha, E. (2010). Inter-species transplantation and migration of primordial germ cells in cyprinid fish. Int. J. Dev. Biol. 54, 1481–1486.
| Inter-species transplantation and migration of primordial germ cells in cyprinid fish.Crossref | GoogleScholarGoogle Scholar | 20979025PubMed |
Saito, T., Goto-Kazeto, R., Kawakami, Y., Nomura, K., Tanaka, H., Adachi, S., Arai, K., and Yamaha, E. (2011). The mechanism for primordial germ-cell migration is conserved between Japanese eel and zebrafish. PLoS One 6, e24460.
| The mechanism for primordial germ-cell migration is conserved between Japanese eel and zebrafish.Crossref | GoogleScholarGoogle Scholar | 21931802PubMed |
Saito, T., Pšenička, M., Goto, R., Adachi, S., Inoue, K., Arai, K., and Yamaha, E. (2014). The origin and migration of primordial germ cells in sturgeons. PLoS One 9, e86861.
| The origin and migration of primordial germ cells in sturgeons.Crossref | GoogleScholarGoogle Scholar | 25546433PubMed |
Saito, T., Güralp, H., Iegorova, V., Rodina, M., and Pšenicka, M. (2018). Elimination of primordial germ cells in sturgeon embryos by ultraviolet irradiation. Biol. Reprod. 99, 556–564.
| Elimination of primordial germ cells in sturgeon embryos by ultraviolet irradiation.Crossref | GoogleScholarGoogle Scholar | 29635315PubMed |
Schwander, T., and Oldroyd, B. P. (2016). Androgenesis: where males hijack eggs to clone themselves. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150534.
| Androgenesis: where males hijack eggs to clone themselves.Crossref | GoogleScholarGoogle Scholar | 27619698PubMed |
Shang, M., Su, B., Perera, D. A., Alsaqufi, A., Lipke, E. A., Cek, S., Dunn, D. A., Qin, Z., Peatman, E., and Dunham, R. A. (2018). Testicular germ line cell identification, isolation, and transplantation in two North American catfish species. Fish Physiol. Biochem. 44, 717–733.
| Testicular germ line cell identification, isolation, and transplantation in two North American catfish species.Crossref | GoogleScholarGoogle Scholar | 29357082PubMed |
Siegfried, K. R., and Nusslein-Volhard, C. (2008). Germ line control of female sex determination in zebrafish. Dev. Biol. 324, 277–287.
| Germ line control of female sex determination in zebrafish.Crossref | GoogleScholarGoogle Scholar | 18930041PubMed |
Silva, M. A., Costa, G. M., Lacerda, S. M., Brandão-Dias, P. F., Kalapothakis, E., Silva Júnior, A. F., Alvarenga, E. R., and França, L. R. (2016). Successful xenogeneic germ cell transplantation from Jundia catfish (Rhamdia quelen) into adult Nile tilapia (Oreochromis niloticus) testes. Gen. Comp. Endocrinol. 230–231, 48–56.
| Successful xenogeneic germ cell transplantation from Jundia catfish (Rhamdia quelen) into adult Nile tilapia (Oreochromis niloticus) testes.Crossref | GoogleScholarGoogle Scholar | 26972155PubMed |
Siripattarapravat, K., Pinmee, B., Venta, P. J., Chang, C. C., and Cibelli, J. B. (2009). Somatic cell nuclear transfer in zebrafish. Nat. Methods 6, 733–735.
| Somatic cell nuclear transfer in zebrafish.Crossref | GoogleScholarGoogle Scholar | 19718031PubMed |
Slanchev, K., Stebler, J., de la Cueva-Mendez, G., and Raz, E. (2005). Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc. Natl Acad. Sci. USA 102, 4074–4079.
| Development without germ cells: the role of the germ line in zebrafish sex differentiation.Crossref | GoogleScholarGoogle Scholar | 15728735PubMed |
Takahashi, E., Shimizu, Y., Urushibata, H., Kawakami, Y., Arai, K., and Yamaha, E. (2017). Migration behavior of PGCs and asymmetrical gonad formation in pond smelt Hypomesus nipponensis. Int. J. Dev. Biol. 61, 397–405.
| Migration behavior of PGCs and asymmetrical gonad formation in pond smelt Hypomesus nipponensis.Crossref | GoogleScholarGoogle Scholar | 28695959PubMed |
Takeuchi, Y., Yoshizaki, G., Kobayashi, T., and Takeuchi, T. (2002). Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter. Biol. Reprod. 67, 1087–1092.
| Mass isolation of primordial germ cells from transgenic rainbow trout carrying the green fluorescent protein gene driven by the vasa gene promoter.Crossref | GoogleScholarGoogle Scholar | 12297522PubMed |
Takeuchi, Y., Yoshizaki, G., and Takeuchi, T. (2003). Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout. Biol. Reprod. 69, 1142–1149.
| Generation of live fry from intraperitoneally transplanted primordial germ cells in rainbow trout.Crossref | GoogleScholarGoogle Scholar | 12773413PubMed |
Tsai, S. (2009). Development of cryopreservation techniques for early stage zebrafish (Danio rerio) oocytes. Ph.D. Thesis, University of Bedfordshire, Luton.
Uribe, M. C., Grier, H. J., and Mejía-Roa, V. (2014). Comparative testicular structure and spermatogenesis in bony fishes. Spermatogenesis 4, e983400.
| Comparative testicular structure and spermatogenesis in bony fishes.Crossref | GoogleScholarGoogle Scholar | 26413406PubMed |
Uribe, M. C., Grier, H. J., García-Alarcón, A., and Parenti, L. R. (2016). Oogenesis: from oogonia to ovulation in the flagfish, Jordanella floridae Goode and Bean, 1879 (Teleostei: Cyprinodontidae. J. Morphol. 277, 1339–1354.
| Oogenesis: from oogonia to ovulation in the flagfish, Jordanella floridae Goode and Bean, 1879 (Teleostei: Cyprinodontidae.Crossref | GoogleScholarGoogle Scholar | 27418385PubMed |
Viana, I. K. S., Gonçalves, L. A. B., Ferreira, M. A. P., Mendes, Y. A., and Rocha, R. M. (2018). Oocyte growth, follicular complex formation and extracellular-matrix remodeling in ovarian maturation of the imperial zebra pleco fish Hypancistrus zebra. Sci. Rep. 8, 13760.
| Oocyte growth, follicular complex formation and extracellular-matrix remodeling in ovarian maturation of the imperial zebra pleco fish Hypancistrus zebra.Crossref | GoogleScholarGoogle Scholar |
Weidinger, G., Slanchev, J. K., Dumstrei, K., Wise, C., Lovell-Badge, R., Thisse, C., Thisse, B., and Raz1, E. (2003). dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr. Biol. 13, 1429–1434.
| dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival.Crossref | GoogleScholarGoogle Scholar | 12932328PubMed |
Weidinger, G., Wolke, U., Köprunner, M., Klinger, M., and Raz, E. (1999). Identification of tissues and patterning events required for distinct steps in early migration of zebrafish primordial germ cells. Development 126, 5295–5307.
| 10556055PubMed |
Wong, T.-T., and Zohar, Y. (2015). Production of reproductively sterile fish by a non-transgenic gene silencing technology. Sci. Rep. 5, 15822.
| Production of reproductively sterile fish by a non-transgenic gene silencing technology.Crossref | GoogleScholarGoogle Scholar | 26510515PubMed |
Wong, T.-T., Saito, T., Crodian, J., and Collodi, P. (2011). Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae. Biol. Reprod. 84, 1190–1197.
| Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae.Crossref | GoogleScholarGoogle Scholar | 21248287PubMed |
Wootton, R. J., and Smith, C. (2014a). Gametogenesis. In ‘Reproductive Biology of Teleost Fishes’ pp. 45–80. (John Wiley & Sons.)
Wootton, R. J., and Smith, C. (2014b). Sex differentiation. In ‘Reproductive Biology of Teleost Fishes’. pp. 31–43. (John Wiley & Sons.)
World Wildlife Fund (WWF) (2015). Living blue planet report. Species, habitats and human well-being. WWF, Gland, Switzerland.
Yamaha, E., Murakami, M., Hada, K., Otani, S., Fujimoto, T., Tanaka, M., Sakao, S., Kimura, S., Sato, S., and Arai, K. (2003). Recovery of fertility in male hybrids of a cross between goldfish and common carp by transplantation of PGC (primordial germ cell)-containing graft. Genetica 119, 121–131.
| 14620952PubMed |
Yamaha, E., Saito, T., Goto-Kazeto, R., and Arai, K. (2007). Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes. J. Sea Res. 58, 8–22.
| Developmental biotechnology for aquaculture, with special reference to surrogate production in teleost fishes.Crossref | GoogleScholarGoogle Scholar |
Yang, H., Carmichael, C., Varga, Z. M., and Tiersch, T. R. (2007). Development of a simplified and standardized protocol with potential for high-throughput for sperm cryopreservation in zebrafish Danio rerio. Theriogenology 68, 128–136.
| Development of a simplified and standardized protocol with potential for high-throughput for sperm cryopreservation in zebrafish Danio rerio.Crossref | GoogleScholarGoogle Scholar | 17544099PubMed |
Ye, H., Li, C. J., Yue, H. M., Du, H., Yang, X. G., Yoshino, T., Hayashida, T., Takeuchi, Y., and Wei, Q. W. (2017). Establishment of intraperitoneal germ cell transplantation for critically endangered Chinese sturgeon Acipenser sinensis. Theriogenology 94, 37–47.
| Establishment of intraperitoneal germ cell transplantation for critically endangered Chinese sturgeon Acipenser sinensis.Crossref | GoogleScholarGoogle Scholar | 28407859PubMed |
Yoon, C., Kawakami, K., and Hopkins, N. (1997). Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124, 3157–3165.
| 9272956PubMed |
Yoshikawa, H., Ino, Y., Shigenaga, K., Katayama, T., Kuroyanagi, M., and Yoshiura, Y. (2018). Production of tiger puffer Takifugu rubripes from cryopreserved testicular germ cells using surrogate broodstock technology. Aquaculture 493, 302–313.
| Production of tiger puffer Takifugu rubripes from cryopreserved testicular germ cells using surrogate broodstock technology.Crossref | GoogleScholarGoogle Scholar |
Yoshizaki, G., and Lee, S. (2018). Production of live fish derived from frozen germ cells via germ cell transplantation. Stem Cell Res. 29, 103–110.
| Production of live fish derived from frozen germ cells via germ cell transplantation.Crossref | GoogleScholarGoogle Scholar | 29649725PubMed |
Yoshizaki, G., Takeuchi, Y., Sakatani, S., and Takeuchi, T. (2000). Germ cell-specific expression of green fluorescent protein in transgenic rainbow trout under control of the rainbow trout vasa-like gene promoter. Int. J. Dev. Biol. 44, 323–326.
| 10853829PubMed |
Yoshizaki, G., Takeuchi, Y., Kobayashi, T., Ihara, S., and Takeuchi, T. (2002). Primordial germ cells: the blueprint for a piscine life. Fish Physiol. Biochem. 26, 3–12.
| Primordial germ cells: the blueprint for a piscine life.Crossref | GoogleScholarGoogle Scholar |
Yoshizaki, G., Tago, Y., Takeuchi, Y., Sawatari, E., Kobayashi, T., and Takeuchi, T. (2005). Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in salmonidae. Biol. Reprod. 73, 88–93.
| Green fluorescent protein labeling of primordial germ cells using a nontransgenic method and its application for germ cell transplantation in salmonidae.Crossref | GoogleScholarGoogle Scholar | 15744027PubMed |
Yoshizaki, G., Ichikawa, M., Hayashi, M., Iwasaki, Y., Miwa, M., Shikina, S., and Okutsu, T. (2010). Sexual plasticity of ovarian germ cells in rainbow trout. Development 137, 1227–1230.
| Sexual plasticity of ovarian germ cells in rainbow trout.Crossref | GoogleScholarGoogle Scholar | 20223765PubMed |
Yoshizaki, G., Okutsu, T., Morita, T., Terasawa, M., Yazawa, R., and Takeuchi, Y. (2012). Biological characteristics of fish germ cells and their application to developmental biotechnology. Reprod. Domest. Anim. 47, 187–192.
| Biological characteristics of fish germ cells and their application to developmental biotechnology.Crossref | GoogleScholarGoogle Scholar | 22827369PubMed |
Yoshizaki, G., Takashiba, K., Shimamori, S., Fujinuma, K., Shikina, S., Okutsu, T., Kume, S., and Hayashi, M. (2016). Production of germ cell-deficient salmonids by dead end gene knockdown, and their use as recipients for germ cell transplantation. Mol. Reprod. Dev. 83, 298–311.
| Production of germ cell-deficient salmonids by dead end gene knockdown, and their use as recipients for germ cell transplantation.Crossref | GoogleScholarGoogle Scholar | 26860442PubMed |