Skip to main content
SpringerLink
Log in

Establishment of four types of allotetraploids derived from Crassostrea gigas and C. angulata and their breeding potential

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Large-scale production of triploid oysters requires tetraploids as broodstock; hence, tetraploidy is a key asset for the triploid oyster industry. To explore the possibility of obtaining new allotetraploid strains with improved traits through hybridization and polyploidization, we conducted a comparative study for growth, survival, and gonadal development of tetraploid Crassostrea gigas, tetraploid C. angulata, and four allotetraploids. Firstly, allotriploid GGA (C. gigas ♀ × C. angulata ♂) and AAG (C. angulata ♀ × C. gigas ♂) were obtained from the hybridization between diploid C. gigas and diploid C. angulata by inhibiting the polar body II. Subsequently, allotetraploid GGGA (triploid C. gigas ♀ × diploid C. angulata ♂), allotetraploid AAAG (triploid C. angulata ♀ × diploid C. gigas ♂), allotetraploid GGAG (allotriploid GGA ♀ × diploid C. gigas ♂), allotetraploid AAGG (allotriploid AAG ♀ × diploid C. gigas ♂), autotetraploid GGGG (triploid C. gigas ♀ × diploid C. gigas ♂), and autotetraploid AAAA (triploid C. angulata ♀ × diploid C. angulata ♂) were obtained by inhibiting polar body I. The growth, survival, and gonad development of six groups (GGGA, AAAG, GGAG, AAGG, GGGG, and AAAA) were assessed. There were no detectable differences in fertilization and hatching rates among the six groups. Flow cytometry analysis showed that the tetraploid ratios of the four allotetraploid groups exceeded 88% on day 20. At larval stage, the allotetraploids GGGA and GGAG groups had higher growth rates and cumulative survival rates than the autotetraploid groups. Field-based phenotyping at three sites indicated that certain allotetraploid groups exhibited higher growth and survival compared to the autotetraploid groups. In particular, the best group over 9 months of testing was the allotetraploid GGAG, which significantly outperformed the autotetraploid groups in growth and survival. Furthermore, most of the individuals from the four allotetraploids were fully mature, with morphologically normal oocytes or sperm. The establishment of these four allotetraploids offers new germplasm resources for oyster genetic improvement and commercial production.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Allen SK, Downing SL (1986) Performance of triploid Pacific oysters, Crassostrea gigas (Thunberg). I. Survival, growth, glycogen content, and sexual maturation in yearlings. J Exp Mar Biol Ecol 102:197–208

    Google Scholar 

  • Allen SK, Erskine AJ, Walker EJ, DeBrosse GA (2005) Production of tetraploid suminoe oysters, Crassostrea ariakensis. Aquaculture 247:3

    Google Scholar 

  • Arai K, Fujimoto T, Wang HP (2018) Chromosome manipulation techniques and applications to aquaculture. In: Piferrer F, Chen SL (eds) Sex Control in Aquaculture. John Wiley & Sons Ltd., pp 137–162

    Google Scholar 

  • Batista FM, Leitão A, Fonseca VG, Ben-Hamadou R, Ruano F, Henriques MA, Guedes-Pinto H, Boudry P (2007) Individual relationship between aneuploidy of gill cells and growth rate in the cupped oysters Crassostrea angulata, C. gigas and their reciprocal hybrids. J Exp Mar Biol Ecol 352:226–233

    Google Scholar 

  • Botta R, Asche F, Borsum JS, Camp EV (2020) A review of global oyster aquaculture production and consumption. Marine Policy 117:103952

    Google Scholar 

  • Boudry P, Heurtebise S, Lapègue S (2003) Mitochondrial and nuclear DNA sequence variation of presumed Crassostrea gigas and Crassostrea angulata specimens: a new oyster species in Hong Kong? Aquaculture 228:15–25

    CAS  Google Scholar 

  • Chen C (2012) Studies on environmental conditions and carrying capacity of Pacific oyster farming sites in Rushan. Ph.D. Dissertation, Ocean University of China, Qingdao, China, pp 13–14 (in Chinese)

    Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482

    CAS  PubMed  Google Scholar 

  • Chen L, Xu J, Sun X, Xu P (2022) Research advances and future perspectives of genomics and genetic improvement in allotetraploid common carp. Rev Aquac 14:957–978

    CAS  Google Scholar 

  • Cheng F, Wu J, Cai X, Liang J, Freeling M, Wang X (2018) Gene retention, fractionation and subgenome differences in polyploid plants. Nat Plants 4:258–268

    CAS  PubMed  Google Scholar 

  • Chourrout D, Chevassus B, Krieg F, Happe A, Burger G, Renard P (1986) Production of second generation triploid and tetraploid rainbow trout by mating tetraploid males and diploid females-potential of tetraploid fish. Theor Appl Genet 72:193–206

    CAS  PubMed  Google Scholar 

  • Dégremont L (2011) Evidence of herpesvirus (OsHV-1) resistance in juvenile Crassostrea gigas selected for high resistance to the summer mortality phenomenon. Aquaculture 317:94–98

    Google Scholar 

  • Dégremont L, Garcia C, Allen SK Jr (2015) Genetic improvement for disease resistance in oysters: a review. J Invertebr Pathol 131:226–241

    PubMed  Google Scholar 

  • Dégremont L, Maurouard E, Ledu C, Benabdelmouna A (2019) Synthesis of the “PLAN DE SAUVEGARDE” using selected all-triploid oysters T to reduce the shortage of spat in France due to OsHV-1–associated mortality in Crassostrea gigas. Aquaculture 505:462–472

    Google Scholar 

  • Eudeline B, Allen SK, Guo X (2000) Optimization of tetraploid induction in Pacific oysters, Crassostrea gigas, using first polar body as a natural indicator. Aquaculture 187:73–84

    Google Scholar 

  • FAO (2022) Global aquaculture production. Fisheries and Aquaculture Division (online), Rome https://www.fao.org/fishery/en/collection/aquaculture?lang=en

    Google Scholar 

  • Farahmand H, Razak SHA, Hwang GL, Maclean N, Rahman MA (2007) Induction of tetraploidy in transgenic tilapia (Oreochromis niloticus) using physical shocks. Iran J Fish Sci 7:27–46

    Google Scholar 

  • Felip A, Piferrer F, Zanuy S, Carrillo M (2001) Comparative growth performance of diploid and triploid European sea bass over the first four spawning seasons. J Fish Biol 58:76–88

    Google Scholar 

  • Gagnaire PA, Lamy JB, Cornette F, Heurtebise S, Degremont L, Flahauw E, Boudry P, Bierne N, Lapegue S (2018) Analysis of genome-wide differentiation between native and introduced populations of the cupped oysters Crassostrea gigas and Crassostrea angulata. Genome Biol Evol 10:2518–2534

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gui J, Liang S, Zhu L, Jiang Y (1993) Discovery of multiple tetraploids in artificially propagated populations of allogynogenetic silver crucian carp and their breeding potentialities. Chin Sci Bull 38:327–331

    Google Scholar 

  • Guo X, Allen SK (1994) Viable tetraploids in the Pacific oyster Crassostrea gigas Thunberg produced by inhibiting polar body I in eggs from triploids. Mol Mar Biol Biotechnol 3:42–50

    Google Scholar 

  • Guo X, DeBrosse GA, Allen SK (1996) All-triploid Pacific oysters (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture 142:149–161

    Google Scholar 

  • Guo X (2012) Production and breeding of tetraploid eastern oyster Crassostrea virginica. J Shellfish Res 31:292

    Google Scholar 

  • Hawkins AJS, Magoulas A, Héral M, Bougrier S, Naciri-Graven Y, Day AJ, Kotoulas G (2000) Separate effects of triploidy, parentage and genomic diversity upon feeding behaviour, metabolic efficiency and net energy balance in the Pacific oyster Crassostrea gigas. Genet Res Camb 76:273–284

    CAS  Google Scholar 

  • He Y, Sun Y, Zheng R, Ai Y, Cao Z, Bao M (2016) Induction of tetraploid male sterile Tagetes erecta by colchicine treatment and its application for interspecific hybridization. Hortic Plant J 2:284–292

    Google Scholar 

  • In VV, O’Connor W, Sang VV, Van PT, Knibb W (2017) Resolution of the controversial relationship between Pacific and Portuguese oysters internationally and in Vietnam. Aquaculture 473:389–399

    Google Scholar 

  • Ibarra AM, Ascenciomichel R, Ramírez JL, Manzanosarabia M, Rodríguezjaramillo C (2017) Performance of diploid and triploid Crassostrea gigas (Thunberg, 1793) grown in tropical versus temperate natural environmental conditions. J Shellfish Res 36:119–139

    Google Scholar 

  • Jiang G, Li Q, Xu C, Liu S, Kong L, Yu H (2021) Reciprocal hybrids derived from Crassostrea gigas and C. angulata exhibit high heterosis in growth, survival and thermotolerance in northern China. Aquaculture 545:737173

    Google Scholar 

  • Jiang G, Li Q, Xu C (2022) Growth, survival and gonad development of two new types of reciprocal triploid hybrids between Crassostrea gigas and C. angulata. Aquaculture 559:738451

    CAS  Google Scholar 

  • Jiang G, Chi C, Zhou J, Cheng G, Du L, Xu C, Li Q (2023) Phenotypic evaluation of two genetically improved strains selected from the reciprocal hybrids of Crassostrea gigas and C. angulata. Aquaculture 576:739808

    Google Scholar 

  • Juchno D, Pecio A, Boroń A, Leska A, Jablonska O, Cejko BI, Kowalski RK, Judycka S, Przybylski M (2017) Evidence of the sterility of allotetraploid Cobitis loaches (Teleostei, Cobitidae) using testes ultrastructure. J Exp Zool 327A:66–74

    Google Scholar 

  • Langdon C, Evans F, Jacobson D, Blouin M (2003) Yields of cultured Pacific oysters Crassostrea gigas Thunberg improved after one generation of selection. Aquaculture 220:227–244

    Google Scholar 

  • Li Q, Wang Q, Liu S, Kong L (2011) Selection response and realized heritability for growth in three stocks of the Pacific oyster Crassostrea gigas. Fish Sci 77:643–648

    CAS  Google Scholar 

  • Li Z, Liang H, Wang Z, Zou G, Gui J (2016) A novel allotetraploid gibel carp strain with maternal body type and growth superiority. Aquaculture 458:55–63

    Google Scholar 

  • Li Y, Li Q (2022) The growth, survival and ploidy of diploid, triploid and tetraploid of the Pacific oyster (Crassostrea gigas) in larval and juvenile stages. Aquaculture 553:738083

    Google Scholar 

  • Lind CE, Evans BS, Knauer J, Taylor JJ, Jerry DR (2009) Decreased genetic diversity and a reduced effective population size in cultured silver-lipped pearl oysters (Pinctada maxima). Aquaculture 286:12–19

    Google Scholar 

  • Liu S, Liu Y, Zhou G, Zhang X, Luo C, Feng H, He X, Zhu G, Yang H (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192:171–186

    Google Scholar 

  • Malison JA, Procarione LS, Held JA, Kayes TB, Amundson CH (1993) The influence of triploidy and heat and hydrostatic pressure shocks on the growth and reproductive development of juvenile yellow perch (Perca flavescens). Aquaculture 116:121–133

    Google Scholar 

  • McCombie H, Ledu C, Phelipot P, Lapègue S, Boudry P, Gérard A (2005) A complementary method for production of tetraploid Crassostrea gigas using crosses between diploids and tetraploids with cytochalasin B treatments. Mar Biotechnol 7:318–330

    CAS  Google Scholar 

  • Menzel RW (1974) Portuguese and Japanese oysters are the same species. J Fish Res Bd Can 31:453–456

    Google Scholar 

  • Miller PA, Elliott NG, Vaillancourt RE, Kube PD, Koutoulis A (2014) Genetic diversity and pedigree assignment in tetraploid Pacific oysters (Crassostrea gigas). Aquaculture 433:318–324

    Google Scholar 

  • Myers JM (1986) Tetraploid induction in Oreochromis spp. Aquaculture 57:281–287

    Google Scholar 

  • Nam YK, Kim DS (2004) Ploidy status of progeny from the crosses between tetraploid males and diploid females in mud loach (Misgurnus mizolepis). Aquaculture 236:575–582

    CAS  Google Scholar 

  • Piferrer F, Beaumont A, Falguière JC, Flajšhans M, Haffray P, Colombo L (2009) Polyploid fish and shellfish: production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture 293:125–156

    Google Scholar 

  • Porta J, Maria Porta J, Cañavate P, Martínez-Rodríguez G, Carmen Alvarez M (2007) Substantial loss of genetic variation in a single generation of Senegalese sole (Solea senegalensis) culture: implications in the domestication process. J Fish Biol 71:223–234

    CAS  Google Scholar 

  • Qin Q, Wang Y, Wang J, Dai J, Xiao J, Hu F, Luo K, Tao M, Zhang C, Liu Y, Liu S (2014) The autotetraploid fish derived from hybridization of Carassius auratus red var. (female) × Megalobrama amblycephala (male). Biol Reprod 91:93

    PubMed  Google Scholar 

  • Reece KS, Cordes JF, Stubbs JB, Hudson KL, Francis EA (2007) Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Mar Biol 153:709–721

    Google Scholar 

  • Soletchnik P, Huvet A, Moine OL, Razet D, Geairon P, Faury N, Goulletquer P, Boudry P (2002) A comparative field study of growth, survival and reproduction of Crassostrea gigas, C. angulata and their hybrids. Aquat Living Resour 15:243–250

    Google Scholar 

  • Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids: do segmental allopolyploids exist? Genome 39:1176–1184

    CAS  PubMed  Google Scholar 

  • Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424

    PubMed  Google Scholar 

  • Wan W, Qin Y, Shi G, Li S, Liao Q, Ma H, Li J, Suo A, Ding D, Yu Z, Zhang Y (2023) Genetic improvement of aquaculture performance for tetraploid Pacific oysters, Crassostrea gigas: a case study of four consecutive generations of selective breeding. Aquaculture 563:738910

    Google Scholar 

  • Wang Z, Guo X, Allen SK, Wang R (2002) Heterozygosity and body size in triploid Pacific oysters, Crassostrea gigas Thunberg, produced from meiosis II inhibition and tetraploids. Aquaculture 204:337–348

    Google Scholar 

  • Wang H, Qian L, Liu X, Zhang G, Guo X (2010) Classification of a common cupped oyster from southern China. J Shellfish Res 29(4):857–866

    Google Scholar 

  • Xu P, Xu J, Liu G, Chen L, Zhou Z, Peng W, Jiang Y, Zhao Z, Jia Z, Sun Y, Wu Y, Chen B, Pu F, Feng J, Luo J, Chai J, Zhang H, Wang H, Dong C et al (2019) The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio. Nat Commun 10:4625

    PubMed  PubMed Central  Google Scholar 

  • Yang H, Simon N, Sturmer L (2018) Production and performance of triploid oysters for aquaculture. University of Florida Institute of Food and Agricultural Sciences. FA208, Gainesville, p 9 http://edis.ifas.ufl.edu/fa208

    Google Scholar 

  • Yang H, Guo X, Scarpa J (2019) Induction and establishment of tetraploid oyster breeding stocks for triploid oyster production. University of Florida Institute of Food and Agricultural Sciences. FA215, Gainesville, p 8 https://edis.ifas.ufl.edu/FA215

    Google Scholar 

  • Yao H, Dogra Gray A, Auger DL, Birchler JA (2013) Genomic dosage effects on heterosis in triploid maize. Proc Natl Acad Sci USA 110:2665–2669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Li Q, Xu C (2018) Estimates of genetic parameters of growth-related traits in Crassostrea gigas ‘Haida no. 1’. J Fish Sci China 25:998–1003 (in Chinese)

    Google Scholar 

  • Zhang Y, Qin Y, Yu Z (2022) Comparative study of tetraploid-based reciprocal triploid Portuguese oysters, Crassostrea angulata, from seed to marketsize. Aquaculture 547:737523

    Google Scholar 

  • Zou S, Li S, Cai W, Zhao J, Yang H (2004) Establishment of fertile tetraploid population of blunt snout bream (Megalobrama amblycephala). Aquaculture 238:155–164

    Google Scholar 

Download references

Funding

This research was supported by grants from the National Key R&D Program of China (2022YFD2400305), Earmarked Fund for Agriculture Seed Improvement Project of Shandong Province (2021ZLGX03, 2022LZGCQY010, and 2020LZGC016), and China Agriculture Research System Project (CARS-49).

Author information

Authors and Affiliations

  1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Gaowei Jiang, Chengxun Xu & Qi Li

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Qi Li

Authors
  1. Gaowei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chengxun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Gaowei Jiang: conceptualization, data curation, formal analysis, methodology, and writing—original draft. Chengxun Xu: supervision and resources. Qi Li: supervision, conceptualization, resources, writing—review and editing, and funding acquisition.

Corresponding author

Correspondence to Qi Li.

Ethics declarations

Ethics approval

The present study was performed according to the standard operation procedures (SOPs) of the Guide for the Use of Experimental Animals of the Ocean University of China. All animal care and use procedures were approved by the Institutional Animal Care and Use Committee of Ocean University of China.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Pierre Boudry

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, G., Xu, C. & Li, Q. Establishment of four types of allotetraploids derived from Crassostrea gigas and C. angulata and their breeding potential. Aquacult Int 32, 4971–4989 (2024). https://doi.org/10.1007/s10499-024-01411-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-024-01411-9

Keywords

Search

Navigation