Skip to main content

Advertisement

Log in

First Genome-wide Association Analysis for Growth Traits in the Largest Coral Reef-Dwelling Bony Fishes, the Giant Grouper (Epinephelus lanceolatus)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The giant grouper, Epinephelus lanceolatus, is the largest coral reef-dwelling bony fish species. However, despite extremely fast growth performance and the considerable economic importance in this species, its genetic regulation of growth remains unknown. Here, we performed the first genome-wide association study (GWAS) for five growth traits in 289 giant groupers using 42,323 single nucleotide polymorphisms (SNPs) obtained by genotyping-by-sequencing (GBS). We identified a total of 36 growth-related SNPs, of which 11 SNPs reached a genome-wide significance level. The phenotypic variance explained by these SNPs varied from 7.09% for body height to 18.42% for body length. Moreover, 22 quantitative trait loci (QTLs) for growth traits, including nine significant QTLs and 13 suggestive QTLs, were found on multiple chromosomes. Interestingly, the QTL (LG17: 6934451) was shared between body weight and body height, while two significant QTLs (LG7: 22596399 and LG15: 11877836) for body length were consistent with the associated regions of total length at the genome-wide suggestive level. Eight potential candidate genes close to the associated SNPs were selected for expression analysis, of which four genes (phosphatidylinositol transfer protein cytoplasmic 1, protein tyrosine phosphatase receptor type E, alpha/beta hydrolase domain-containing protein 17C, and vascular endothelial growth factor A-A) were differentially expressed and involved in metabolism, development, response stress, etc. This study improves our understanding of the complex genetic architecture of growth in the giant grouper. The results contribute to the selective breeding of grouper species and the conservation of coral reef fishes.

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

Access this article

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Ahmad F, Azevedo JL, Cortright R, Dohm GL, Goldstein BJ (1997) Alterations in skeletal muscle protein-tyrosine phosphatase activity and expression in insulin-resistant human obesity and diabetes. J Clin Invest 100:449–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bak A, Jacob AI, Aga-Mizrachi S, Brutman-Barazani T, Sampson SR, Elson A (2008) Cytosolic protein tyrosine phosphatase-ε is a negative regulator of insulin signaling in skeletal muscle. Endocrinology 149:605–614

    Article  CAS  PubMed  Google Scholar 

  • Baker KD, Ramel MC, Lekven AC (2010) A direct role for Wnt8 in ventrolateral mesoderm patterning. Dev Dyn 239:2828–2836

  • Barría A, Christensen KA, Yoshida GM, Correa K, Jedlicki A, Lhorente JP, Davidson WS, Yáñez JM (2018) Genomic predictions and genome-wide association study of resistance against Piscirickettsia salmonis in coho salmon (Oncorhynchus kisutch) using ddRAD sequencing. G3 (Bethesda) 8:1183–1194

    Article  CAS  Google Scholar 

  • Bharadwaj MS, Zhou Y, Molina AJ, Criswell T, Lu B (2014) Examination of bioenergetic function in the inner mitochondrial membrane peptidase 2-like (Immp2l) mutant mice. Redox Biol 2:1008–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonferroni C (1936) Teoria statistica delle classi e calcolo delle probabilita. Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commericiali di Firenze 8:3–62

    Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Campbell NR, Lapatra SE, Overturf K, Towner R, Narum SR (2014) Association mapping of disease resistance traits in rainbow trout using restriction site associated DNA sequencing. G3 (Bethesda) 4:2473–2481

    Article  Google Scholar 

  • Chan PY, Han X, Zheng B, Deran M, Yu J, Jarugumilli GK, Deng H, Pan D, Luo X, Wu X (2016) Autopalmitoylation of TEAD proteins regulates transcriptional output of the Hippo pathway. Nat Chem Biol 12:282–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A (2009) Adipogenesis and WNT signalling. Trends Endocrin Met 20:16–24

    Article  CAS  Google Scholar 

  • Cockcroft S (2007) Trafficking of phosphatidylinositol by phosphatidylinositol transfer proteins. Biochem Soc Symp 74:259–271

    Article  CAS  Google Scholar 

  • Craig MT, Sadovy de Mitcheson YJ, Heemstra PC (2011) Groupers of the world: a field and market guide. Grahamstown, South Africa

    Google Scholar 

  • Dong L, Xiao S, Chen J, Wan L, Wang Z (2016) Genomic selection using extreme phenotypes and pre-selection of SNPs in large yellow croaker (Larimichthys crocea). Mar Biotechnol (NY) 18:575–583

    Article  CAS  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farcy E, Serpentini A, Fievet B, Lebel J (2007) Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comp Biochem Physiol B Biochem Mol Biol 146:540–550

    Article  CAS  PubMed  Google Scholar 

  • Geng X, Sha J, Liu S, Bao L, Zhang J, Wang R, Yao J, Li C, Feng J, Sun F, Sun L, Jiang C, Zhang Y, Chen A, Dunham R, Zhi D, Liu Z (2015) A genome-wide association study in catfish reveals the presence of functional hubs of related genes within QTLs for columnaris disease resistance. BMC Genomics 16:196

    Article  PubMed  PubMed Central  Google Scholar 

  • Geng X, Liu S, Yao J, Bao L, Zhang J, Li C, Wang R, Sha J, Zeng P, Zhi D (2016) A genome-wide association study identifies multiple regions associated with head size in catfish. G3 (Bethesda) 6:3389–3398

    Article  CAS  Google Scholar 

  • Geng X, Liu S, Yuan Z, Jiang Y, Zhi D, Liu Z (2017) A genome-wide association study reveals that genes with functions for bone development are associated with body conformation in catfish. Mar Biotechnol 19:570–578

    Article  CAS  Google Scholar 

  • Gjedrem T (2012) Genetic improvement for the development of efficient global aquaculture: a personal opinion review. Aquaculture 344-349:12–22

    Article  Google Scholar 

  • Gonzalez-Pena D, Gao G, Baranski M, Moen T, Cleveland BM, Kenney PB, Vallejo RL, Palti Y, Leeds TD (2016) Genome-wide association study for identifying loci that affect fillet yield, carcass, and body weight traits in rainbow trout (Oncorhynchus mykiss). Front Genet 7:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu XH, Jiang DL, Huang Y, Li BJ, Chen CH, Lin HR, Xia JH (2018) Identifying a major QTL associated with salinity tolerance in Nile tilapia using QTL-Seq. Mar Biotechnol 20:98–107

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Helyar SJ, Hemmer-Hansen J, Bekkevold D, Taylor M, Ogden R, Limborg M, Cariani A, Maes G, Diopere E, Carvalho G (2011) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Mol Ecol Resour 11:123–136

    Article  PubMed  Google Scholar 

  • Huang YZ, Zou Y, Lin Q, He H, Zheng L, Zhang ZJ, Dang YL, Lei CZ, Lan XY, Qi XS, Chen H (2017) Effects of genetic variants of the bovine WNT8A gene on nine important growth traits in beef cattle. J Genet 96:535–544

    Article  CAS  PubMed  Google Scholar 

  • Jiang DL, Gu XH, Li BJ, Zhu ZX, Qin H, Meng ZN, Lin HR, Xia JH (2019) Identifying a long QTL cluster across chrLG18 associated with salt tolerance in tilapia using GWAS and QTL-seq. Mar Biotechnol. https://doi.org/10.1007/s10126-019-09877-y

  • Jin Y, Zhou T, Geng X, Liu S, Chen A, Yao J, Jiang C, Tan S, Su B, Liu Z (2017) A genome-wide association study of heat stress-associated SNPs in catfish. Anim Genet 48:233–236

    Article  CAS  PubMed  Google Scholar 

  • Kessuwan K, Kubota S, Liu Q, Sano M, Okamoto N, Sakamoto T, Yamashita H, Nakamura Y, Ozaki A (2016) Detection of growth-related quantitative trait loci and high-resolution genetic linkage maps using simple sequence repeat markers in the kelp grouper (Epinephelus bruneus). Mar Biotechnol 18:57–84

    Article  CAS  Google Scholar 

  • Kubota S, Longloy A, Singhabun A, Khammee W, Kessuwan K, Bunlipatanon P, Ozaki A, Silapajarn K, Tanasomwang V, Okamoto N, Sakamoto T (2017) Quantitative trait locus mapping of growth-related traits in inter-specific F1 hybrid grouper (Epinephelus fuscoguttatus × E. lanceolatus) in a tropical climate. Aquac Res 48:5913–5927

    Article  CAS  Google Scholar 

  • Lalitha S (2000) Primer Premier 5. Biotech Software, Internet Report 1:270–272

    Article  Google Scholar 

  • Lavides MN, Polunin NVC, Stead SM, Tabaranza DG, Comeros MT, Dongallo JR (2009) Finfish disappearances around Bohol, Philippines inferred from traditional ecological knowledge. Environ Conserv 36:235–244

    Article  Google Scholar 

  • Lavides MN, Molina EP, Jr DLRG, Mill AC, Rushton SP, Stead SM, Polunin NV (2016) Patterns of coral-reef finfish species disappearances inferred from fishers’ knowledge in global epicentre of marine shorefish diversity. PLoS One 11:e0155752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, Laneve P, Rajewsky N, Bozzoni I (2017) Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell 66:22–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Zhou T, Geng X, Jin Y, Wang X, Liu S, Xu X, Gao D, Li Q, Liu Z (2018) Identification of novel genes significantly affecting growth in catfish through GWAS analysis. Mol Genet Genomics 293:1–13

    Article  CAS  Google Scholar 

  • Li BJ, Zhu ZX, Gu XH, Lin HR, Xia JH (2019) QTL mapping for red blotches in Malaysia red tilapia (Oreochromis spp.). Mar Biotechnol. https://doi.org/10.1007/s10126-019-09888-9

  • Liang D, Chang JR, Chin AJ, Smith A, Kelly C, Weinberg ES, Ge R (2001) The role of vascular endothelial growth factor (VEGF) in vasculogenesis, angiogenesis, and hematopoiesis in zebrafish development. Mech Dev 108:29–43

    Article  CAS  PubMed  Google Scholar 

  • Liu ZJ, Cordes J (2004) DNA marker technologies and their applications in aquaculture genetics. Aquaculture 238:1–37

    Article  CAS  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577

    Article  CAS  PubMed  Google Scholar 

  • Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nathan B, Katsutoshi G, Carsten S, Gerhard W, Jocelyn L, Schafer CA, Berman SS, Michael K, Zon LI (2007) Duplicate VegfA genes and orthologues of the KDR receptor tyrosine kinase family mediate vascular development in the zebrafish. Blood 110:3627–3636

    Article  CAS  Google Scholar 

  • Nguyen NH, Rastas PMA, Premachandra HKA, Knibb W (2018) First high-density linkage map and single nucleotide polymorphisms significantly associated with traits of economic importance in yellowtail kingfish Seriola lalandi. Front Genet 9:693

    Google Scholar 

  • Otrock ZK, Mahfouz RR, Makarem JA, Shamseddine AI (2007) Understanding the biology of angiogenesis: review of the most important molecular mechanisms. Blood Cells Mol Dis 39:212–220

    Article  CAS  PubMed  Google Scholar 

  • Palaiokostas C, Kocour M, Prchal M, Houston RD (2018) Accuracy of genomic evaluations of juvenile growth rate in common carp (Cyprinus carpio) using genotyping by sequencing. Front Genet 9:82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinton CD, Mcmillan I, Glebe BD (2005) Development of an Atlantic salmon (Salmo salar) genetic improvement program: genetic parameters of harvest body weight and carcass quality traits estimated with animal models. Aquaculture 247:211–217

    Article  Google Scholar 

  • Randall JE (1995) Coastal fishes of Oman. Bathurst, Australia

    Google Scholar 

  • Robledo D, Matika O, Hamilton A, Houston RD (2018) Genome-wide association and genomic selection for resistance to amoebic gill disease in Atlantic salmon. G3 (Bethesda) 4:1195–1203

    Article  CAS  Google Scholar 

  • Rosenberg NA, Huang L, Jewett EM, Szpiech ZA, Jankovic I, Boehnke M (2010) Genome-wide association studies in diverse populations. Nat Rev Genet 11:356–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salem M, Al-Tobasei R, Ali A, Lourenco D, Gao G, Palti Y, Kenney B, Leeds TD (2018) Genome-wide association analysis with a 50K transcribed gene SNP-chip identifies QTL affecting muscle yield in rainbow trout. Front Genet 9:387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salisbury BA, Pungliya M, Choi JY, Jiang R, Sun XJ, Stephens JC (2003) SNP and haplotype variation in the human genome. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 526:53–61

    Article  CAS  PubMed  Google Scholar 

  • Sang JW, Kit MCS, Martin BR (2018) Protein depalmitoylases. Crit Rev Biochem Mol Biol 53:83–98

    Article  CAS  Google Scholar 

  • Schaid DJ, Chen W, Larson NB (2018) From genome-wide associations to candidate causal variants by statistical fine-mapping. Nat Rev Genet 19:491–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spinelli M, Fusco S, Grassi C (2018) Nutrient-dependent changes of protein palmitoylation: impact on nuclear enzymes and regulation of gene expression. Int J Mol Sci 19:3820

    Article  CAS  PubMed Central  Google Scholar 

  • Sun Y, Guo C-Y, Wang D-D, Li XF, Xiao L, Zhang X, You X, Shi Q, Hu G-J, Fang C, Lin H-R, Zhang Y (2016) Transcriptome analysis reveals the molecular mechanisms underlying growth superiority in a novel grouper hybrid (Epinephelus fuscogutatus♀ × E. lanceolatus♂). BMC Genet 17:24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai HY, Hamilton A, Tinch AE, Guy DR, Gharbi K, Stear MJ, Matika O, Bishop SC, Houston RD (2015) Genome wide association and genomic prediction for growth traits in juvenile farmed Atlantic salmon using a high density SNP array. BMC Genomics 16:969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaughan LK, Wiener HW, Aslibekyan S, Allison DB, Havel PJ, Stanhope KL, O’brien DM, Hopkins SE, Lemas DJ, Boyer BB (2015) Linkage and association analysis of obesity traits reveals novel loci and interactions with dietary n-3 fatty acids in an Alaska Native (Yup’ik) population. Metab Clin Exp 64:689–697

    Article  CAS  PubMed  Google Scholar 

  • Visscher PM, Wray NR, Zhang Q, Sklar P, Mccarthy MI, Brown MA, Yang J (2017) 10 years of GWAS discovery: biology, function, and translation. Am J Hum Genet 101:5–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vonnahme KA, Wilson ME, Li Y, Rupnow HL, Phernetton TM, Ford SP, Magness RR (2005) Circulating levels of nitric oxide and vascular endothelial growth factor throughout ovine pregnancy. J Physiol 565:101–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Misztal I, Aguilar I, Legarra A, Fernando RL, Vitezica Z, Okimoto R, Wing T, Hawken R, Muir WM (2014) Genome-wide association mapping including phenotypes from relatives without genotypes in a single-step (ssGWAS) for 6-week body weight in broiler chickens. Front Genet 5:134

    PubMed  PubMed Central  Google Scholar 

  • Wang X, Liu X, Deng D, Mei Y, Li X (2016) Genetic determinants of pig birth weight variability. BMC Genet 17:S15

    Article  CAS  Google Scholar 

  • Wang L, Liu P, Huang SQ, Ye BQ, Chua E, Wan ZY, Yue GH (2017a) Genome-wide association study identifies loci associated with resistance to viral nervous necrosis disease in Asian seabass. Mar Biotechnol 19:255–265

    Article  CAS  Google Scholar 

  • Wang X, Liu S, Jiang C, Geng X, Zhou T, Li N, Bao L, Li Y, Yao J, Yang Y, Zhong X, Jin Y, Dunham R, Liu Z (2017b) Multiple across-strain and within-strain QTLs suggest highly complex genetic architecture for hypoxia tolerance in channel catfish. Mol Gen Genomics 292:63–76

    Article  CAS  Google Scholar 

  • Williams KC (2009) A review of feeding practices and nutritional requirements of postlarval groupers. Aquaculture 292:141–152

    Article  CAS  Google Scholar 

  • Yang S, Wang L, Zhang Y, Liu XC, Lin HR, Meng ZN (2011) Development and characterization of 32 microsatellite loci in the giant grouper Epinephelus lanceolatus (Serranidae). Genet Mol Res 10:4006–4011

    Article  CAS  PubMed  Google Scholar 

  • Yu H, You X, Li J, Liu H, Meng Z, Xiao L, Zhang H, Lin HR, Zhang Y, Shi Q (2016) Genome-wide mapping of growth-related quantitative trait loci in orange-spotted grouper (Epinephelus coioides) using double digest restriction-site associated DNA sequencing (ddRADseq). Int J Mol Sci 17:501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, You X, Li J, Zhang X, Zhang S, Jiang S, Lin X, Lin HR, Meng Z, Shi Q (2018) A genome-wide association study on growth traits in orange-spotted grouper (Epinephelus coioides) with RAD-seq genotyping. Sci China Life Sci 61:934–946

    Article  CAS  PubMed  Google Scholar 

  • Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15:376–396

    Article  Google Scholar 

  • Yue G, Wang L (2017) Current status of genome sequencing and its applications in aquaculture. Aquaculture 468:337–347

    Article  CAS  Google Scholar 

  • Zhong X, Wang X, Zhou T, Jin Y, Tan S, Jiang C, Geng X, Li N, Shi H, Zeng Q, Yang Y, Yuan Z, Bao L, Liu S, Tian C, Peatman E, Li Q, Liu Z (2017) Genome-wide association study reveals multiple novel QTL associated with low oxygen tolerance in hybrid catfish. Mar Biotechnol (NY) 19:379–390

    Article  CAS  Google Scholar 

  • Zhou Z, Chen L, Dong C, Peng W, Kong S, Sun J, Pu F, Chen B, Feng J, Xu P (2018) Genome-scale association study of abnormal scale pattern in yellow river carp identified previously known causative gene in European mirror carp. Mar Biotechnol 20:573–583

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the referees and editor for their valuable comments and suggestions, as well as careful corrections of our manuscript. We thank Dr. Leyun Zheng (Fisheries Research Institute of Fujian) for providing fish samples.

Sequence Data Accession

The sequencing data have been deposited into the DDBJ sequence read archive (DRA) with BioProject no. PRJDB8251.

Funding

This research was funded by the Science and Technology Planning Project of Guangzhou (201804020013), the Special Fund for Agro-scientific Research in the Public Interest (201403008), the National Natural Science Foundation of China (31872572), and the Modern Agriculture Talents Support Program (2016–2020).

Author information

Authors and Affiliations

Authors

Contributions

L.W. and Z.M. designed the study. X.W. and W.H. collected the samples. L.W. and Z.M. performed the laboratory work. L.W., Y.Y., and B.L. performed the analyses. J.X. contributed technical assistance. L.W. and Z.M. drafted the paper. X.L. and Z.M. contributed reagents/materials/analysis tools.

Corresponding author

Correspondence to Zining Meng.

Ethics declarations

All experiments in the present study were approved by the Animal Care and Use Committee in the Life Sciences School of Sun Yet-Sen University.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

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

Electronic Supplementary Material

Fig. S1

Frequency of SNPs in different structural attributes of genic and intergenic regions (PNG 130 kb)

High Resolution Image (TIF 212 kb)

Fig. S2

Frequency distribution of different traits in giant grouper (PNG 90 kb)

High Resolution Image (TIF 377 kb)

Fig. S3

Correlation heatmap between different characteristics (PNG 170 kb)

High Resolution Image (TIF 733 kb)

Fig. S4

Population genetic relatedness among the 289 fishes. The genetic relatedness showed that most of the values are distributed at the levels of 0~0.5 (blue region) (PNG 558 kb)

High Resolution Image (TIF 2001 kb)

Fig. S5

QQ plots of the p values in GWAS analysis using GLM and MLM models for (a) total length (TL), (b) body length (BL), (c) body height (BH), (d) body thickness (BT), (e) body weight (BW) (PNG 204 kb)

High Resolution Image (TIF 1343 kb)

Fig. S6

QQ plots of the p values in GWAS analysis using the MLM model for (a) total length (TL), (b) body length (BL), (c) body height (BH), (d) body thickness (BT), (e) body weight (BW) (TIF 1127 kb) (PNG 159 kb)

High Resolution Image (TIF 1127 kb)

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 18 kb)

ESM 3

(FA 34031 kb)

ESM 4

(DOCX 18 kb)

ESM 5

(DOCX 23 kb)

ESM 6

(DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, L., Yang, Y., Li, B. et al. First Genome-wide Association Analysis for Growth Traits in the Largest Coral Reef-Dwelling Bony Fishes, the Giant Grouper (Epinephelus lanceolatus). Mar Biotechnol 21, 707–717 (2019). https://doi.org/10.1007/s10126-019-09916-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09916-8

Keywords

Profiles

  1. Xi Wang