Molecular Parentage Analysis in Aquaculture: Principles, Applications, and Challenges: A Review

Seyed Ehsan Vesal *

Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale, Naples-80121, Italy.

*Author to whom correspondence should be addressed.


Abstract

Molecular parentage analysis is a powerful tool for reconstructing pedigrees and estimating genetic parameters in aquaculture species. It is based on the comparison of DNA marker genotypes between offspring and potential parents. This review provides a concise overview of molecular parentage analysis in aquaculture, covering its principles, methods, applications, challenges, and limitations. It describes common DNA markers, including microsatellites and single nucleotide polymorphisms (SNPs), used in parentage analysis and the criteria for their selection. The software and statistical methods for assigning parentage and evaluating the accuracy and power of the assignment are also discussed. This review demonstrates applications for estimating genetic parameters, investigating inbreeding, evaluating reproductive success, and improving selective breeding programs. In conclusion, while molecular parentage analysis is a valuable tool for improving genetic management in aquaculture, careful planning, implementation, and interpretation are essential.

Keywords: Molecular parentage, aquaculture, DNA markers, selective breeding, genetic parameters, breeding programs


How to Cite

Vesal, S. E. (2024). Molecular Parentage Analysis in Aquaculture: Principles, Applications, and Challenges: A Review. Asian Journal of Fisheries and Aquatic Research, 26(3), 62–75. https://doi.org/10.9734/ajfar/2024/v26i3747

Downloads

Download data is not yet available.

References

Naylor R, Fang S, Fanzo J. A global view of aquaculture policy. Food Policy. 2023; 116:102422.

Azra MN, Okomoda VT, Ikhwanuddin M. Breeding technology as a tool for sustainable aquaculture production and ecosystem services. Frontiers in Marine Science. 2022;9:679529.

Su G, Sørensen AC, Chu TT, Meier K, Nielsen T, Lund MS. Impact of phenotypic information and composition of reference population on genomic prediction in fish under the presence of genotype by environment interaction. Aquaculture. 2020;526:735358.

D’Agaro E, Favaro A, Matiussi S, Gibertoni PP, Esposito S. Genomic selection in salmonids: New discoveries and future perspectives. Aquaculture International. 2021;29(5):2259-89.

Herbinger CM, Doyle RW, Pitman ER, Paquet D, Mesa KA, Morris DB, Wright JM, Cook D. DNA fingerprint based analysis of paternal and maternal effects on offspring growth and survival in communally reared rainbow trout. Aquaculture. 1995;137(1-4):245-56.

Jones AG, Small CM, Paczolt KA, Ratterman NL. A practical guide to methods of parentage analysis. Molecular Ecology Resources. 2010;10(1):6-30.

Avise JC. Molecular markers, natural history and evolution. Springer Science & Business Media; 2012.

Vandeputte M, Haffray P. Parentage assignment with genomic markers: a major advance for understanding and exploiting genetic variation of quantitative traits in farmed aquatic animals. Frontiers in genetics. 2014;5:118682.

Liu T, Li Q, Kong L, Yu H. Comparison of microsatellites and SNPs for pedigree analysis in the Pacific oyster Crassostrea gigas. Aquaculture International. 2017;25: 1507-19.

Houston RD, Taggart JB, Cézard T, Bekaert M, Lowe NR, Downing A, Talbot R, Bishop SC, Archibald AL, Bron JE, Penman DJ. Development and validation of a high density SNP genotyping array for Atlantic salmon (Salmo salar). BMC Genomics. 2014;15:1-3.

Liu P, Xia JH, Lin G, Sun F, Liu F, Lim HS, Pang HY, Yue GH. Molecular parentage analysis is essential in breeding Asian seabass. PloS One. 2012;7(12):e51142.

Wang CM, Lo LC, Zhu ZY, Lin G, Feng F, Li J, Yang WT, Tan J, Chou R, Lim HS, Orban L. Estimating reproductive success of brooders and heritability of growth traits in Asian sea bass (Lates calcarifer) using microsatellites. Aquaculture Research. 2008;39(15):1612-9.

Paul K, D'Ambrosio J, Phocas F. Temporal and region‐specific variations in genome‐wide inbreeding effects on female size and reproduction traits of rainbow trout. Evolutionary Applications. 2022; 15(4):645-62.

Frost AR, Schofield CP, Beaulah SA, Mottram TT, Lines JA, Wathes CM. A review of livestock monitoring and the need for integrated systems. Computers and Electronics in Agriculture. 1997; 17(2):139-59.

Norris D, McQueen JM, Cutler A. Merging information in speech recognition: Feedback is never necessary. Behavioral and Brain Sciences. 2000;23(3):299-325.

Jones AG, Ardren WR. Methods of parentage analysis in natural populations. Molecular Ecology. 2003;12(10):2511-23.

Jones AG, Small CM, Paczolt KA, Ratterman NL. A practical guide to methods of parentage analysis. Molecular Ecology Resources. 2010;10(1):6-30.

Levin N, Heimowitz A. Mapping spatial and temporal patterns of Mediterranean wildfires from MODIS. Remote Sensing of Environment. 2012;126:12-26.

Yue GH, Orban L. A simple and affordable method for high‐throughput DNA extraction from animal tissues for polymerase chain reaction. Electrophoresis. 2005;26(16): 3081-3.

Wenne R. Microsatellites as molecular markers with applications in exploitation and conservation of aquatic animal populations. Genes. 2023;14(4):808.

Vieira ML, Santini L, Diniz AL, Munhoz CD. Microsatellite markers: What they mean and why they are so useful. Genetics and Molecular Biology. 2016;39:312-28.

Vandeputte M, Rossignol MN, Pincent C. From theory to practice: empirical evaluation of the assignment power of marker sets for pedigree analysis in fish breeding. Aquaculture. 2011; 314(1-4): 80-6.

Wong J, Sun F, Wang L, Yang ZT, Wen YF, Pang HY, Lee M, Yeo ST, Liang B, Chen K, Jiang JH. Changes in genetic diversity of Asian seabass in a 20-year breeding program. Aquaculture. 2023;575: 739738.

Xu J, Feng J, Peng W, Liu X, Feng J, Xu P. Development and evaluation of a high‐throughput single nucleotide polymorphism multiplex assay for assigning pedigrees in common carp. Aquaculture Research. 2017;48(4): 1866-76.

Saillant E, Dupont-Nivet M, Haffray P, Chatain B. Estimates of heritability and genotype–environment interactions for body weight in sea bass (Dicentrarchus labrax L.) raised under communal rearing conditions. Aquaculture. 2006; 254 (1-4):139-47.

Borrell A, Aguilar A, Gazo M, Kumarran RP, Cardona L. Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environmental Biology of Fishes. 2011;92:559-67.

Hauser SR, Ding ZM, Getachew B, Toalston JE, Oster SM, McBride WJ, et al. The posterior ventral tegmental area mediates alcohol-seeking behavior in alcohol-preferring rats. J Pharmacol Exp Ther. 2011;336:857–65.

Lien S, Gidskehaug L, Moen T, Hayes BJ, Berg PR, Davidson WS, Omholt SW, Kent MP. A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics. 2011;12:1-0.

Liu F, Sun F, Li J, Xia JH, Lin G, Tu RJ, Yue GH. A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci. BMC Genomics. 2013;14:1-4.

Sellars MJ, Dierens L, McWilliam S, Little B, Murphy B, Coman GJ, Barendse W, Henshall J. Comparison of microsatellite and SNP DNA markers for pedigree assignment in Black Tiger shrimp, Penaeus monodon. Aquaculture Research. 2014;45(3):417-26.

Grashei KE, Ødegård J, Meuwissen THE. Using genomic relationship likelihood for parentage assignment. Genet Sel. 2018; 50(26). Available:https://doi.org/10.1186/s12711-018-0397-7

Kalinowski ST, Taper ML, Marshall TC. Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment. Molecular Ecology. 2007;16(5):1099-106.

Taggart JB. FAP: An exclusion‐based parental assignment program with enhanced predictive functions. Molecular Ecology Notes. 2007;7(3):412-5.

Valière N. GIMLET: A computer program for analysing genetic individual identification data. Molecular Ecology Notes. 2002;2(3):377-9.

Vandeputte M, Mauger S, Dupont‐Nivet M. An evaluation of allowing for mismatches as a way to manage genotyping errors in parentage assignment by exclusion. Molecular Ecology Notes. 2006;6(1):265-7.

Yue G, Li Y, Chen F, Cho S, Lim LC, Orban L. Comparison of three DNA marker systems for assessing genetic diversity in Asian arowana (Scleropages formosus). Electrophoresis. 2002;23(7‐8):1025-32.

Chamberlain JS. Multiple PCR for the diagnosis of duchenne muscular dystrophy. PCR protocols: A guide to methods and applicationsl. 1990: 272-81.

Diyie RL, Aheto DW, Osei-Atweneboana MY, Armah E, Yankson K. Prevalence of bacterial infections and the use of multiplex PCR assay for rapid detection of pathogens in cultured fish in Ghana. Archives of Microbiology. 2022;204(7):394.

Delamare-Deboutteville J, Meemetta W, Pimsannil K, Sangpo P, Gan HM, Mohan CV, Dong HT, Senapin S. A multiplexed RT-PCR assay for nanopore whole genome sequencing of Tilapia lake virus (TiLV). Scientific Reports. 2023;13(1): 20276.

Yue J, Hartsough MT, Frey RS, Frielle T, Mulder KM. Cloning and expression of a rat Smad1: Regulation by TGFß and modulation by the ras/MEK pathway. Journal of Cellular Physiology. 1999; 178(3):387-96.

Ferraro RR, Marks GF. The development of SSM/I rain-rate retrieval algorithms using ground-based radar measurements. Journal of Atmospheric and Oceanic Technology. 1995;12(4):755-70.

Vemireddy LR, Archak S, Nagaraju J. Capillary electrophoresis is essential for microsatellite marker based detection and quantification of adulteration of Basmati rice (Oryza sativa) J Agric Food Chem. 2007;55:8112–811.

Ziegle JS, Su Y, Corcoran KP, Nie L, Mayrand PE, Hoff LB, McBride LJ, Kronick MN, Diehl SR. Application of automated DNA sizing technology for genotyping microsatellite loci. Genomics. 1992;14(4): 1026-31.

Sánchez-Velásquez JJ, Reyes-Flores LE, Yzásiga-Barrera C, Zelada-Mázmela E. Performance comparison of gel and capillary electrophoresis-based microsatellite genotyping strategies in a population research and kinship testing framework. BMC Research Notes. 2021; 14:1-8.

Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ. Current trends in microsatellite genotyping. Molecular Ecology Resources. 2011;11(4):591-611.

Bártfai R, Egedi S, Yue GH, Kovács B, Urbányi B, Tamás G, Horváth L, Orbán L. Genetic analysis of two common carp broodstocks by RAPD and microsatellite markers. Aquaculture. 2003;219(1-4): 157-67.

Sekino M, Kakehi S. PARFEX v1. 0: an EXCEL™-based software package for parentage allocation. Conservation Genetics Resources. 2012;4:275-8.

Duchesne P, Godbout MH, Bernatchez L. PAPA (package for the analysis of parental allocation): A computer program for simulated and real parental allocation. Molecular Ecology Notes. 2002;2(2):191-3.

Jones OR, Wang J. Colony: A program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources. 2010;10(3):551-5.

Al-Shuhaib MB, Hashim HO. Mastering DNA chromatogram analysis in Sanger sequencing for reliable clinical analysis. Journal of Genetic Engineering and Biotechnology. 2023;21(1):115.

Ishihara S, Kotomura N, Yamamoto N, Ochiai H. Ligation-mediated PCR with a back-to-back adapter reduces amplification bias resulting from variations in GC content. Analytical Biochemistry. 2017; 531:37-44.

Reece JS, Bowen BW, Joshi K, Goz V, Larson A. Phylogeography of two moray eels indicates high dispersal throughout the Indo-Pacific. Journal of Heredity. 2010;101(4):391-402.

Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P. Micro‐Checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes. 2004;4(3):535-8.

Doubleday ZA, Semmens JM, Smolenski AJ, Shaw PW. Microsatellite DNA markers and morphometrics reveal a complex population structure in a merobenthic octopus’s species (Octopus maorum) in south-east Australia and New Zealand. Marine Biology. 2009;156(6):1183-92.

Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AV. Automated binning of microsatellite alleles: Problems and solutions. Molecular Ecology Notes. 2007; 7(1):10-4.

Ellis JS, Gilbey J, Armstrong A, Balstad T, Cauwelier E, Cherbonnel C, Consuegra S, Coughlan J, Cross TF, Crozier W, Dillane E. Microsatellite standardization and evaluation of genotyping error in a large multi-partner research programme for conservation of Atlantic salmon (Salmo salar L.). Genetica. 2011;139: 353-67.

Skaarud A, Woolliams JA, Gjøen HM. Strategies for controlling inbreeding in fish breeding programs; an applied approach using optimum contribution (OC) procedures. Aquaculture. 2011;311(1-4):110-4.

Nielsen EE, Hansen MM, Bach LA. Looking for a needle in a haystack: Discovery of indigenous Atlantic salmon (Salmo salar L.) in stocked populations. Conservation Genetics. 2001;2:219-32.

Olesen I, Bentsen HB, Phillips M, Ponzoni RW. Can the global adoption of genetically improved farmed fish increase beyond 10% and how? Journal of Marine Science and Engineering. 2015 May 19;3(2): 240-66.

Glover KA, Pertoldi C, Besnier F, Wennevik V, Kent M, Skaala Ø. Atlantic salmon populations invaded by farmed escapees: Quantifying genetic introgression with a Bayesian approach and SNPs. BMC Genetics. 2013;14:1-9.

Vandeputte M, Dupont-Nivet M, Chatain B, Chevassus B. Setting up a strain-testing design for the seabass, Dicentrarchus labrax: a simulation study. Aquaculture. 2001;202(3-4):329-42.

Dupont-Nivet G, Butler RF, Yin A, Robinson D, Zhang Y, Qiao WS. Paleomagnetism on arcuate structures along the Altyn Tagh fault: Implications for the intracontinental deformation processes in Asia. Eos Trans. AGU. 2001;82.

Sae-Lim P, Komen H, Kause A. Bias and precision of estimates of genotype-by-environment interaction: A simulation study. Aquaculture. 2010; 310(1-2): 66-73.

Bass S. Temperature effects and genotype-temperature interactions on sex determination in the European. Journal of Experimental, Zoology. 2002;292:494-505.

DOI: 10.1002/jez.10071

Lane SN, November V, Landström C, Whatmore S. Explaining rapid transitions in the practice of flood risk management. Annals of the Association of American Geographers. 2013;103(2):330-42.

Kocour, Martin, Otomar Linhart, and Marc Vandeputte. Mouth and fin deformities in common carp: Is there a genetic basis?. 2006;419-422. Available:https://doi.org/10.1111/j.1365-2109.2005.01425.x

Norris AT, Cunningham EP. Estimates of phenotypic and genetic parameters for flesh colour traits in farmed Atlantic salmon based on multiple trait animal model. Livestock Production Science. 2004;89(2-3):209-22.

Vieira Antônio Robério, Carlos Bôa-Viagem Rabello M. Do CMM Ludke, wilson moreira dutra júnior, delma maria torres, and joão batista lopes. Effect of Different Inclusion Levels of Rice Bran in Diets Supplemented with Phytase for Broiler Chickens. 2007;267-275.

Lavelle D, Bardon A. E-tendering in construction: Time for a change?. Northumbria Working Paper Series: Interdisciplinary Studies in the Built and Virtual Environment. 2009;2(2):104-12.

Antonello J, Massault C, Franch R, Haley C, Pellizzari C, Bovo G, Patarnello T, de Koning DJ, Bargelloni L. Estimates of heritability and genetic correlation for body length and resistance to fish pasteurellosis in the gilthead sea bream (Sparus aurata L.). Aquaculture. 2009;298(1-2):29-35.

DOI: 10.1016/j.aquaculture.2009.10.022

Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B. A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics. 2007;176(2):1049-57.

Nguyen TT, Hayes BJ, Ingram BA. Genetic parameters and response to selection in blue mussel (Mytilus galloprovincialis) using a SNP-based pedigree. Aquaculture. 2014;420:295-301.

Haffray P, Vandeputte M, Petit V, Pincent C, Chatain B, Chapuis H, Mériaux JC, Coudurier B, Quillet E, Dupont-Nivet M. Minimizing maternal effect in salmonid families mixed since eyed stages and a posteriori DNA-pedigreed. Livestock Science. 2012;150(1-3):170-8.

Ninh NH, Ponzoni RW, Nguyen NH, Woolliams JA, Taggart JB, McAndrew BJ, Penman DJ. A comparison of communal and separate rearing of families in selective breeding of common carp (Cyprinus carpio): Estimation of genetic parameters. Aquaculture. 2011;322:39-46.

Ferrari S, Chatain B, Cousin X, Leguay D, Vergnet A, Vidal MO, Vandeputte M, Begout ML. Early individual electronic identification of sea bass using RFID microtags: A first example of early phenotyping of sex-related growth. Aquaculture. 2014;426:165-71.

Houston RD, Taggart JB, Cézard T, Bekaert M, Lowe NR, Downing A, Talbot R, Bishop SC, Archibald AL, Bron JE, Penman DJ. Development and validation of a high density SNP genotyping array for Atlantic salmon (Salmo salar). BMC genomics. 2014;15:1-3.

Meuwissen T, Goddard M. Accurate prediction of genetic values for complex traits by whole-genome resequencing. Genetics. 2010;185(2):623-31.

Sonesson AK, Meuwissen TH. Testing strategies for genomic selection in aquaculture breeding programs. Genetics Selection Evolution. 2009;41:1-9.

Palaiokostas C, Bekaert M, Davie A, Cowan ME, Oral M, Taggart JB, Gharbi K, McAndrew BJ, Penman DJ, Migaud H. Mapping the sex determination locus in the Atlantic halibut (Hippoglossus hippoglossus) using RAD sequencing. BMC genomics. 2013; 14:1-2.

Li, Yanxia, Michael Fetchko, Zhi-Chun Lai, and Nicholas E. Baker. Scabrous and Gp150 are endosomal proteins that regulate Notch activity. 2003;2819-2827.

Morton R, Howarth JM. Estimation of breeding values using selected pedigree records. Biometrics. 2005;61(2):422-32.

Sonesson AK, Gjerde B, Robinson N. A simple selection scheme to improve disease resistance and growth. Aquaculture. 2011;319(3-4):337-41.

DOI: 10.1016/j.aquaculture.2011.07.009.

Loughnan SR, Domingos JA, Smith-Keune C, Forrester JP, Jerry DR, Beheregaray LB, Robinson NA. Broodstock contribution after mass spawning and size grading in barramundi (Lates calcarifer, Bloch). Aquaculture. 2013;404:139-49.

Dupont-Nivet M, Chevassus B, Mauger S, Haffray P, Vandeputte M. Side effects of sexual maturation on heritability estimates in rainbow trout (Oncorhynchus mykiss). Aquaculture Research. 2010;41(11).

Zenger KR, Khatkar MS, Jones DB, Khalilisamani N, Jerry DR, Raadsma HW. Genomic selection in aquaculture: Application, limitations and opportunities with special reference to marine shrimp and pearl oysters. Front Genet. 2019; 9:693.

DOI: 10.3389/fgene.2018.00693. PMID: 30728827; PMCID: PMC6351666.

Haffray P, Bugeon J, Rivard Q, Quittet B, Puyo S, Allamelou JM, Vandeputte M, Dupont-Nivet M. Genetic parameters of in-vivo prediction of carcass, head and fillet yields by internal ultrasound and 2D external imagery in large rainbow trout (Oncorhynchus mykiss). Aquaculture. 2013;410:236-44.

Vesal SE, Vosooghi AR. Evaluating the effect of dietary soybean oil on growth performances of juvenile severum (Heros severus). Iranian Journal of Fisheries Sciences. 2017;16(3):1030-1042.

Vesal SE, Vosooghi AR. Growth parameters in juvenile gold severum (Heros severus) fed diets containing fish oil and soybean oil. International Journal of Aquatic Science. 2017;8(1):9-15.

Shen X, Yang G, Liao M. Development of 51 genomic microsatellite DNA markers of guppy (Poecilia reticulata) and their application in closely related species. Molecular Ecology Notes. 2007;7(2):302-6.

Melo AT, Hale I. apparent: A simple and flexible R package for accurate SNP-based parentage analysis in the absence of guiding information. BMC Bioinformatics. 2019; 20: 1-0.

Yue GH, Xia JH. Practical considerations of molecular parentage analysis in fish. Journal of the World Aquaculture Society. 2014;45(2):89-103.