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Developmental potential of somatic and germ cells of hybrids between Carassius auratus females and Hemigrammocypris rasborella males

Published online by Cambridge University Press:  10 August 2020

Yuki Naya ,
Tomoka Matsunaga ,
Yu Shimizu ,
Eisuke Takahashi ,
Fumika Shima ,
Mitsuru Endoh ,
Takafumi Fujimoto Open the ORCID record for Takafumi Fujimoto [Opens in a new window] ,
Katsutoshi Arai  and
Etsuro Yamaha Open the ORCID record for Etsuro Yamaha [Opens in a new window]
Yuki Naya
Affiliation:
Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University Laboratory of Aquaculture Genetics and Genomics, Faculty of Fisheries Sciences, Hokkaido University
Tomoka Matsunaga
Affiliation:
Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University
Yu Shimizu
Affiliation:
Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University Laboratory of Aquaculture Genetics and Genomics, Faculty of Fisheries Sciences, Hokkaido University
Eisuke Takahashi
Affiliation:
Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University
Fumika Shima
Affiliation:
Laboratory of Aquaculture Genetics and Genomics, Faculty of Fisheries Sciences, Hokkaido University
Mitsuru Endoh
Affiliation:
Laboratory of Aquaculture Genetics and Genomics, Faculty of Fisheries Sciences, Hokkaido University
Takafumi Fujimoto
Affiliation:
Laboratory of Aquaculture Genetics and Genomics, Faculty of Fisheries Sciences, Hokkaido University
Katsutoshi Arai
Affiliation:
Institute for the Advancement of Higher Education, Hokkaido University
Etsuro Yamaha*
Affiliation:
Nanae Fresh-Water Station, Field Science Center for Northern Biosphere, Hokkaido University
*
Author for correspondence: Etsuro Yamaha. 2-9-1, Sakura, Nanae, Kameda, Hokkaido, 041-1105, Japan. Tel: +81 138-65-2344. Fax: +81 138-65-2239. E-mail: [email protected]
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Summary

The cause of hybrid sterility and inviability has not been analyzed in the fin-fish hybrid, although large numbers of hybridizations have been carried out. In this study, we produced allo-diploid hybrids by cross-fertilization between female goldfish (Carassius auratus) and male golden venus chub (Hemigrammocypris rasborella). Inviability of these hybrids was due to breakage of the enveloping layer during epiboly or due to malformation with serious cardiac oedema around the hatching stage. Spontaneous allo-triploid hybrids with two sets of the goldfish genome and one set of the golden venus chub genome developed normally and survived beyond the feeding stage. This improved survival was confirmed by generating heat-shock-induced allo-triploid hybrids that possessed an extra goldfish genome. When inviable allo-diploid hybrid cells were transplanted into goldfish host embryos at the blastula stage, these embryos hatched normally, incorporating the allo-diploid cells. These allo-diploid hybrid cells persisted, and were genetically detected in a 6-month-old fish. In contrast, primordial germ cells taken from allo-diploid hybrids and transplanted into goldfish hosts at the blastula stage had disappeared by 10 days post-fertilization, even under chimeric conditions. In allo-triploid hybrid embryos, germ cells proliferated in the gonad, but had disappeared by 10 weeks post-fertilization. These results showed that while hybrid germ cells are inviable even in chimeric conditions, hybrid somatic cells remain viable.

Keywords

ChimeraFertilityHybridPolyploidSterility
Type
Research Article
Information
Zygote , Volume 28 , Issue 6 , December 2020 , pp. 470 - 481
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Arai, K (1984). Developmental genetic studies on salmonids: morphogenesis, isozyme phenotypes and chromosome in hybrid embryos. Mem Fac Fish Hokkaido Univ 31, 1–91.Google Scholar
Arai, K (1986). Effect of allotriploidization on development of the hybrids between female chum salmon and male brook trout. Bull Japan Soc Sci Fish 52, 823–9.CrossRefGoogle Scholar
Arai, K (1988). Viability of allotriploids in salmonids. Nippon Suisan Gakkaishi 54, 1695–701.CrossRefGoogle Scholar
Arai, K (2000). Chromosome manipulation in aquaculture: recent progress and perspective. Suisanzosyoku 48, 295–303.Google Scholar
Arai, K (2001). Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 198(1–4), 205–28.CrossRefGoogle Scholar
Arai, K and Fujimoto, T (2019). Chromosome manipulation techniques and applications to aquaculture. In Sex control in Aquaculture, volume I, First Edition (eds Wang, HP, Piferrer, F, Chen, SL and Shen, ZG) John Wiley & Sons Ltd, pp. 137–62.Google Scholar
Blanc, JM and Chevassus, B (1979). Interspecific hybridization of salmonid fish. I. Hatching and survival up to the 15th day after hatching in F1 generation hybrids. Aquaculture 18, 21–34.CrossRefGoogle Scholar
Capanna, E, Cataudella, S and Volpe, R (1974). Unibrido intergenerico tra trota iridea e salmerino di fonte (Salmo gairdneri × Salvelinus fontinalis). Boll Pesca Piscic Idrobiol 29, 101–6.Google Scholar
Chevassus, B, Guyomard, R, Chourrout, D and Quillet, E (1983). Production of viable hybrids in salmonids by triploidization. Genet Sel Evol 15, 519–532.10.1186/1297-9686-15-4-519CrossRefGoogle ScholarPubMed
Devlin, RH and Nagahama, Y (2002). Review article sex determination and sex differentiation in fish: and overview of genetic, physiological, and environmental influences. Aquaculture 208(3–4), 191–364.CrossRefGoogle Scholar
Fujimoto, T, Kataoka, T, Sakao, S, Saito, T, Yamaha, E and Arai, K (2006). Developmental stages and germ cell lineage of the loach (Misgurnus anguillicaudatus). Zool Sci 23, 977–89.CrossRefGoogle Scholar
Fujiwara, A, Abe, S, Yamaha, E, Yamazaki, F and Yoshida, MC (1997). Uniparental chromosome elimination in the early embryogenesis of the inviable salmonid hybrids between masu salmon female and rainbow trout male. Chromosoma 106, 44–52.CrossRefGoogle ScholarPubMed
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(10–12), 465–70.CrossRefGoogle ScholarPubMed
Goto-Kazeto, 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.CrossRefGoogle Scholar
Gray, AK, Evans, MA and Thorgaard, GH (1993). Viability and development of diploid and triploid salmonid hybrids. Aquaculture 112(2–3), 125–42.CrossRefGoogle Scholar
Habibi, HR, Nelson, ER and Allan, ER (2012). New insights into thyroid hormone function and modulation of reproduction in goldfish. Gen Comp Endocrinol 175, 19–26.CrossRefGoogle ScholarPubMed
Hulata, G (2001). Genetic manipulations in aquaculture: a review of stock improvement by classical and modern technologies. Genetica 111, 155–73.CrossRefGoogle ScholarPubMed
Kazama-Wakabayashi, M, Yamaha, E and Yamazaki, F (1999). The elimination and duplication of lower part of blastoderm effects on the number of primordial germ cells in goldfish. Fisher Sci 65, 577–82.CrossRefGoogle Scholar
Kijima, K, Arai, K and Suzuki, R (1996a). Induced allotriploidy in inviable interfamilial hybrids, female loach × male goldfish and female loach × male minnow. J Fac Appl Biol Sci Hiroshima Univ 35, 1–12.Google Scholar
Kijima, K, Arai, K and Suzuki, R (1996b). Induction of allo-triploids and allopentaploids in interfamilial hybrids, female spinous loach × male carp and female loach × male carp. J Fac Appl Biol Sci Hiroshima Univ 35, 13–26.Google Scholar
Labbé, C, Robles, V and Herraez, MP (2017). Epigenetics in fish gametes and early embryo. Aquaculture 472, 93–106.10.1016/j.aquaculture.2016.07.026CrossRefGoogle Scholar
Li, S, Xie, L, Xiao, J, Yuan, L, Zhou, T, Luo, K, Zhang, C, Zhao, R, Tao, M and Liu, S (2019). Diploid hybrid fish derived from the cross between female bleeker’s yellow tail and male topmouth culter, two cyprinid fishes belonging to different subfamilies. BMC Genetics 20, 80.CrossRefGoogle ScholarPubMed
Lin, F, Xu, S, Ma, D, Xiao, Z, Zhao, C, Xiao, Y, Chi, L, Liu, Q and Li, J (2012). Germ line specific expression of a vasa homologue gene in turbot (Scophthalmus maximus): evidence for vasa localization at cleavage furrow in Euteleostei. Mol Reprod Dev 79, 803–13.CrossRefGoogle Scholar
Makino, S, Ojima, Y and Matsui, Y (1958). Cytogenetical and cytochemical studies in carp-funa hybrids. Nucleus 1, 153–62.Google Scholar
Márián, T and Krasznai, A (1978). Karyological investigations on Ctenopharyngodon idella and Hypophthalmichthys molitrix and their cross-breeding. Aquacult Hung 1, 44–50.Google Scholar
Nagasawa, K, Femandes, JMO, Yoshizaki, G and Babiak, I (2013). Identification and migration of primordial germ cells in Atlantic salmon, Salmo salar. Characterization of vasa dead end, and lymphocyte antigen 75 genes. Mol Reprod Dev 80, 118–31.CrossRefGoogle ScholarPubMed
Nagoya, H, Kimoto, T and Onozato, H (1990). Diploid gynogenesis induced by suppression of the second or the third cleavage in the goldfish, Carassius auratus . Bull Natl Res Inst Aquacul 18, 1–6.Google Scholar
Ojima, Y (1973). Fish cytogenetics. Suiko-sha. Tokyo, 453 pp.Google Scholar
Otani, S, Maegawa, S, Inoue, K, Arai, K and Yamaha, E (2002). The germ cell lineage identified by vas-mRNA during the embryogenesis in goldfish. Zool Sci 19, 519–26.CrossRefGoogle ScholarPubMed
Parsons, JE, Busch, RA, Thorgaard, GH and Scheerer, PD (1986). Increased resistance of triploid rainbow trout × coho salmon hybrids to infectious hematopoietic necrosis virus. Aquaculture 57, 337–43.CrossRefGoogle Scholar
Purdom, CE and Lincoln, RF (1974). Gynogenesis in hybrids within Pleuronectidae. In The Early Life History of Fish (ed. Blaxter, JHS), Springer-Verlag, Berlin, 1974, pp. 537–44.CrossRefGoogle Scholar
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, 691–9.CrossRefGoogle ScholarPubMed
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, 159–66.CrossRefGoogle ScholarPubMed
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, 1481–6.CrossRefGoogle ScholarPubMed
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 59, e86861.CrossRefGoogle Scholar
Scheerer, PD and Thorgaard, GH (1983). Increased resistance of triploid rainbow trout x coho salmon. Can J Fish Aquat Sci 40, 2040–4.10.1139/f83-235CrossRefGoogle Scholar
Scribner, KT, Page, KS and Bartron, ML (2001). Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev Fish Biol Fisher 10, 293–323.CrossRefGoogle Scholar
Seeb, JE, Thorgaard, GH and Utter, FM (1988). Survival and allozyme expression in diploid and triploid hybrids between chum, chinook, and coho salmon. Aquaculture 72, 31–48.CrossRefGoogle Scholar
Stanley, JG (1976). Production of hybrid, androgenetic, and gyonogenetic grass carp and carp. Trans Am Fish Soc 105, 10–6.2.0.CO;2>CrossRefGoogle Scholar
Suzuki, R (1956). A study on the interfamiliar crossing between minnow (Gnathopogon elongatus elongatus) and mud loach (Misgurunus anguilicaudatus). Bull Aichi Gakugei Univ V, 29–34.Google Scholar
Suzuki, R (1961). External characters of artificial intergeneric hybrids among Japanese bitterlings (cyprinid fish). Bull Jap Soc Sci Fish xxvii, 418–24.CrossRefGoogle Scholar
Suzuki, R (1962). Hybridization experiments in cyprinid fishes, I. Gnathopogon elongatus elongatus female × Pseudorasbora parva male and the reciprocal. Bull Jap Soc Sci Fish xxviii, 992–7.CrossRefGoogle Scholar
Suzuki, R (1968). Hybridization experiments in cyprinid fishes. XI. Survival rate of F1 hybrids with special reference to the closeness of taxonomical position of combined fishes. Bull Freshwater Fish Res Lab 18, 113–55.Google Scholar
Suzuki, R (1974). Inter-crossing and back-crossing of F1 hybrids among salmonid fishes. Bull Freshwater Fish Res Lab 24, 11–31.Google Scholar
Suzuki, R and Fukuda, Y (1971). Survival potential of F1 hybrids among salmonid fishes. Bull Freshwater Fish Res Lab 21, 69–83.Google Scholar
Suzuki, R and Fukuda, Y (1973). Sexual maturity of F1 hybrids among salmonid fishes. Bull Freshwater Fish Res Lab 23, 57–74.Google Scholar
Swartz, FJ (1981). World literature to fish hybrids with an analysis by family, species, and hybrid: Supplement 1. NOAA Technical Report NMFS SSRF, 750.Google Scholar
Tanaka, M, Yamaha, E and Arai, K (2004). Survival capacity of haploid-diploid goldfish chimeras. J Exp Zool A Comp Exp Biol 301, 491–501.CrossRefGoogle ScholarPubMed
Thorgaard, GH (1983). Chromosome set manipulation and sex control. In Fish Physiology (eds Hoar, WS, Randall, DJ and Donaldson, EM), Vol. 9, Part B, Academic Press, New York, pp. 405–44.Google Scholar
Tsai, HY, Chang, M, Liu, SC, Abe, G and Ota, KG (2013). Embryonic development of goldfish (Carassius auratus): A model for the study of evolutionary change in developmental mechanisms by artificial selection. Dev Dyn 232, 1262–83.CrossRefGoogle Scholar
Ueda, T, Ojima, Y, Sato, R and Fukuda, Y (1984). Triploid hybrids between female rainbow trout and male brook trout. Nippon Suisan Gakkaishi 50, 1331–6.CrossRefGoogle Scholar
Urushibata, H, Takahashi, E, Shimizu, Y, Miyazaki, T, Fujimoto, T, Arai, K and Yamaha, E (2019). Morphological differences in embryos of goldfish (Carassius auratus auratus) under different incubation temperatures. Int J Dev Biol 63, 597–604.CrossRefGoogle ScholarPubMed
Uyeno, T (1972). Chromosomes of offspring resulting from crossing coho salmon and brook trout. Jpn J Ichthyol 19, 166–71.Google Scholar
Yamaha, E and Yamazaki, F (1993). Electrically fused-egg induction and its development in the goldfish, Carassius auratus . Int J Dev Biol 37, 291–8.Google ScholarPubMed
Yamaha, E, Mizuno, T, Hasebe, Y and Yamazaki, F (1997). Chimeric fish produced by exchanging upper parts of blastoderms in goldfish blastulae. Fisheries Sci 63, 514–9.CrossRefGoogle Scholar
Yamaha, E, Kazama-Wakabayashi, M, Otani, S, Fujimoto, T and Arai, K (2001). Germ-line chimera by lower-part blastoderm transplantation between diploid goldfish and triploid crucian carp. Genetica 111(1–3), 227–36.CrossRefGoogle Scholar
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, 121–31.CrossRefGoogle ScholarPubMed
Yamaki, M, Kawakami, K, Taniura, K and Arai, K (1999). Live haploid-diploid mosaic charr Salvelinus leucomaenis . Fisher Sci 65, 736–41.CrossRefGoogle Scholar
Yamano, K, Yamaha, E and Yamazaki, F (1988). Increased viability of allotriploid pink salmon × Japanese char hybrids. Bull Jap Soc Sci Fisheries 54, 1477–81.10.2331/suisan.54.1477CrossRefGoogle Scholar
Yanagimachi, R, Harumi, T, Matsubara, H, Yan, W, Yuan, S, Hirohashi, N, Iida, T, Yamaha, E, Arai, K, Matsubara, T, Andoh, T and Vines, CN (2017). Chemical and physical guidance of fish spermatozoa into the egg through the micropyle. Biol Reprod 96, 780–99.CrossRefGoogle Scholar
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, 3157–65.Google ScholarPubMed
Yoshikawa, H, Xu, D, Ino, Y, Hayashida, T, Wang, J, Yazawa, R, Yoshizaki, G and Takeuchi, Y (2018). Hybrid sterility in fish caused by mitotic arrest of primordial germ cells. Genetics 209, 507–21.CrossRefGoogle ScholarPubMed
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