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RESEARCH ARTICLE

Phenotypic causal networks between boar taint compounds measured in biopsies and carcasses

Margareth Evangelista Botelho https://orcid.org/0000-0001-8746-2272 A B * , Marcos Soares Lopes C D , Pramod K. Mathur C , Egbert F. Knol C , Daniele B. D. Marques https://orcid.org/0000-0001-7080-7465 A , Paulo Sávio Lopes A , Fabyano Fonseca e Silva A , Simone Eliza Facioni Guimarães A and Renata Veroneze A
+ Author Affiliations
- Author Affiliations

A Departament of Animal Science from Universidade Federal de Viçosa, Vicosa 36570-999, Brazil.

B Present address: Empresa de Pesquisa Agropecuária de Minas Gerais, Instituto Tecnológico de Agropecuária de Pitangui, Pitangui 35650-000, Brazil.

C Topigs Norsvin Research Center, Beuningen 6641 SZ, Netherlands.

D Topigs Norsvin, Curitiba, PR 80420-210, Brazil.

* Correspondence to: eb_margareth@yahoo.com.br

Handling Editor: Frank Dunshea

Animal Production Science 63(3) 291-300 https://doi.org/10.1071/AN21277
Submitted: 20 May 2021  Accepted: 26 September 2022   Published: 28 October 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Boar taint compounds (androstenone, skatole and indole) can be measured in pig carcasses, after slaughter or, alternatively, in biopsies of subcutaneous adipose tissue from selected living pigs. Measuring these compounds via biopsy enables data collection in selected animals and high standardisation regarding tissue-collection procedures for phenotyping. Because different analytical methods can be used to measure boar taint compounds, it is important to better understand the relationship between boar taint compounds measured in biopsies and in carcasses.

Aims: This research aimed to identify the causal relationship and causal effects among boar taint compounds (androstenone, skatole and indole) measured in pig adipose tissue from carcasses and biopsies.

Methods: The concentrations of androstenone (AC), skatole (SC) and indole (IC) measured in adipose tissue from pig carcasses and the concentrations of androstenone (AB), skatole (SB) and indole (IB) measured in biopsies were used to fit a multi-trait Structural Equation Model (SEM) considering causal network graphs obtained via inductive causation algorithm with or without a priori information. Models were compared using the deviance information criterion (DIC).

Key results: The best DIC was obtained in a model with a causal structure built using a priori information; however, this model was considered inappropriate, because it returned several null genetic correlations among traits described as positively correlated. The best structure returned using only inductive causation algorithm was IB → SC ← AB ← AC ← SB: SC → IC, which was obtained with an 80–70% high-probability distribution interval. This model returned positive genetic correlations and improved goodness-of-fit compared with the multi-trait model in all cases. Several causal relationships among boar taint compounds in carcasses and biopsies were identified.

Conclusion: Boar taint compounds measured in biopsies have direct effects on boar taint compounds measured in carcasses.

Implications: Knowledge concerning the causal structure of boar taint compounds may be used in breeding programs, helping in the formulation of selection indexes and improving the ability for prediction and selection of this complex trait (boar taint).

Keywords: androstenone, biopsy, boar taint, carcass, causal structure, IC algorithm, indole, skatole.


References

Aluwé M, Millet S, Bekaert KM, Tuyttens FAM, Vanhaecke L, De Smet S, De Brabander DL (2011) Influence of breed and slaughter weight on boar taint prevalence in entire male pigs. Animal 5, 1283–1289.
Influence of breed and slaughter weight on boar taint prevalence in entire male pigs.Crossref | GoogleScholarGoogle Scholar |

Ampuero Kragten S, Verkuylen B, Dahlmans H, Hortos M, Garcia-Regueiro JA, Dahl E, Andresen O, Feitsma H, Mathur PK, Harlizius B (2011) Inter-laboratory comparison of methods to measure androstenone in pork fat. Animal 5, 1634–1642.
Inter-laboratory comparison of methods to measure androstenone in pork fat.Crossref | GoogleScholarGoogle Scholar |

Ayalew G (2019) A review on the effect of immunocastration against gonadal physiology and boar taint. Biomedicine and Nursing 5, 26–40.
A review on the effect of immunocastration against gonadal physiology and boar taint.Crossref | GoogleScholarGoogle Scholar |

Baes C, Mattei S, Luther H, Ampuero S, Sidler X, Bee G, Spring P, Hofer A (2013) A performance test for boar taint compounds in live boars. Animal 7, 714–720.
A performance test for boar taint compounds in live boars.Crossref | GoogleScholarGoogle Scholar |

Bouwman AC, Valente BD, Janss LLG, Bovenhuis H, Rosa GJM (2014) Exploring causal networks of bovine milk fatty acids in a multivariate mixed model context. Genetics Selection Evolution 46, 2
Exploring causal networks of bovine milk fatty acids in a multivariate mixed model context.Crossref | GoogleScholarGoogle Scholar |

Claus R, Weiler U, Herzog A (1994) Physiological aspects of androstenone and skatole formation in the boar – a review with experimental data. Meat Science 38, 289–305.
Physiological aspects of androstenone and skatole formation in the boar – a review with experimental data.Crossref | GoogleScholarGoogle Scholar |

de Campos CF, Lopes MS, e Silva FF, Veroneze R, Knol EF, Sávio Lopes P, Guimarães SEF (2015) Genomic selection for boar taint compounds and carcass traits in a commercial pig population. Livestock Science 174, 10–17.
Genomic selection for boar taint compounds and carcass traits in a commercial pig population.Crossref | GoogleScholarGoogle Scholar |

Duijvesteijn N, Knol EF, Merks JWM, Crooijmans RPMA, Groenen MAM, Bovenhuis H, Harlizius B (2010) A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6. BMC Genetics 11, 42
A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6.Crossref | GoogleScholarGoogle Scholar |

França LR, Avelar GF, Almeida FFL (2005) Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63, 300–318.
Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs.Crossref | GoogleScholarGoogle Scholar |

Gianola D, Sorensen D (2004) Quantitative genetic models for describing simultaneous and recursive relationships between phenotypes. Genetics 167, 1407–1424.
Quantitative genetic models for describing simultaneous and recursive relationships between phenotypes.Crossref | GoogleScholarGoogle Scholar |

Grindflek E, Meuwissen THE, Aasmundstad T, Hamland H, Hansen MHS, Nome T, Kent M, Torjesen P, Lien S (2011) Revealing genetic relationships between compounds affecting boar taint and reproduction in pigs. Journal of Animal Science 89, 680–692.
Revealing genetic relationships between compounds affecting boar taint and reproduction in pigs.Crossref | GoogleScholarGoogle Scholar |

Jayachandran M, Okano H, Chatrath R, Owen WG, McConnell JP, Miller VM (2004) Sex-specific changes in platelet aggregation and secretion with sexual maturity in pigs. Journal of Applied Physiology 97, 1445–1452.
Sex-specific changes in platelet aggregation and secretion with sexual maturity in pigs.Crossref | GoogleScholarGoogle Scholar |

Jensen MT, Cox RP, Jensen BB (1995) 3-Methylindole (skatole) and indole production by mixed populations of pig fecal bacteria. Applied and Environmental Microbiology 61, 3180–3184.
3-Methylindole (skatole) and indole production by mixed populations of pig fecal bacteria.Crossref | GoogleScholarGoogle Scholar |

Lee GJ, Archibald AL, Law AS, Lloyd S, Wood J, Haley CS (2005) Detection of quantitative trait loci for androstenone, skatole and boar taint in a cross between Large White and Meishan pigs. Animal Genetics 36, 14–22.
Detection of quantitative trait loci for androstenone, skatole and boar taint in a cross between Large White and Meishan pigs.Crossref | GoogleScholarGoogle Scholar |

Mathur PK, ten Napel J, Bloemhof S, Heres L, Knol EF, Mulder HA (2012) A human nose scoring system for boar taint and its relationship with androstenone and skatole. Meat Science 91, 414–422.
A human nose scoring system for boar taint and its relationship with androstenone and skatole.Crossref | GoogleScholarGoogle Scholar |

Mathur PK, ten Napel J, Crump RE, Mulder HA, Knol EF (2013) Genetic relationship between boar taint compounds, human nose scores, and reproduction traits in pigs. Journal of Animal Science 91, 4080–4089.
Genetic relationship between boar taint compounds, human nose scores, and reproduction traits in pigs.Crossref | GoogleScholarGoogle Scholar |

Misztal I, Tsuruta S, Lourenco D, Aguilar I, Legarra A, Vitezica Z (2015) ‘Manual for BLUPF90 family of programs.’ (University of Georgia: Athens, GA, USA). Available at http://nce.ads.uga.edu/wiki/lib/exe/fetch.php?media=blupf90_all2.pdf

Pearl J (2003) ‘Causality: models, reasoning, and inference’. ‘Econometric Theory.’ pp. 675–685. (Cambridge University Press). https://doi.org/
| Crossref |

R Core Team (2017) ‘R: a language and environment for statistical computing.’ R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.

Rius MA, Hortós M, García-Regueiro JA (2005) Influence of volatile compounds on the development of off-flavours in pig back fat samples classified with boar taint by a test panel. Meat Science 71, 595–602.
Influence of volatile compounds on the development of off-flavours in pig back fat samples classified with boar taint by a test panel.Crossref | GoogleScholarGoogle Scholar |

Rosa GJM, Valente BD, de los Campos G, Wu X-L, Gianola D, Silva MA (2011) Inferring causal phenotype networks using structural equation models. Genetics Selection Evolution 43, 6
Inferring causal phenotype networks using structural equation models.Crossref | GoogleScholarGoogle Scholar |

Schumacker RE, Lomax RG (2010) ‘A beginner’s guide to structural equation modeling.’ (Ed. RG Lomax) (Taylor & Francis Group: New York, NY, USA)

Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 64, 583–639.
Bayesian measures of model complexity and fit.Crossref | GoogleScholarGoogle Scholar |

Tajet H, Andresen Ø, Meuwissen T (2006) Estimation of genetic parameters of boar taint; skatole and androstenone and their correlations with sexual maturation. Acta Veterinaria Scandinavica 48, S9
Estimation of genetic parameters of boar taint; skatole and androstenone and their correlations with sexual maturation.Crossref | GoogleScholarGoogle Scholar |

ten Napel J, Mathur PK, Mulder HA, Knol EF (2014) Genetic control of skatole in intact boars is dependent on the actual androstenone level. In ‘10th World Congress of genetics applied to livestock production genetic’.Vancouver, Canada 2014. Abstract: 366.

Valente BD, Rosa GJM (2013) Mixed effects structural equation models and phenotypic causal networks. Methods in Molecular Biology 1019, 449–464.
Mixed effects structural equation models and phenotypic causal networks.Crossref | GoogleScholarGoogle Scholar |

Valente BD, Rosa GJM, de Los Campos G, Gianola D, Silva MA (2010) Searching for recursive causal structures in multivariate quantitative genetics mixed models. Genetics 185, 633–644.
Searching for recursive causal structures in multivariate quantitative genetics mixed models.Crossref | GoogleScholarGoogle Scholar |

Valente BD, Rosa GJM, Silva MA, Teixeira RB, Torres RA (2011) Searching for phenotypic causal networks involving complex traits: an application to European quail. Genetics Selection Evolution 43, 37
Searching for phenotypic causal networks involving complex traits: an application to European quail.Crossref | GoogleScholarGoogle Scholar |

Valente BD, Rosa GJM, Gianola D, Wu X-L, Weigel K (2013) Is structural equation modeling advantageous for the genetic improvement of multiple traits? Genetics 194, 561–572.
Is structural equation modeling advantageous for the genetic improvement of multiple traits?Crossref | GoogleScholarGoogle Scholar |

Verheyden K, Noppe H, Aluwé M, Millet S, Vanden Bussche J, De Brabander HF (2007) Development and validation of a method for simultaneous analysis of the boar taint compounds indole, skatole and androstenone in pig fat using liquid chromatography–multiple mass spectrometry. Journal of Chromatography A 1174, 132–137.
Development and validation of a method for simultaneous analysis of the boar taint compounds indole, skatole and androstenone in pig fat using liquid chromatography–multiple mass spectrometry.Crossref | GoogleScholarGoogle Scholar |

Wesoly R, Jungbluth I, Stefanski V, Weiler U (2015) Pre-slaughter conditions influence skatole and androstenone in adipose tissue of boars. Meat Science 99, 60–67.
Pre-slaughter conditions influence skatole and androstenone in adipose tissue of boars.Crossref | GoogleScholarGoogle Scholar |

Wilberg MJ, Bence JR (2008) Performance of deviance information criterion model selection in statistical catch-at-age analysis. Fisheries Research 93, 212–221.
Performance of deviance information criterion model selection in statistical catch-at-age analysis.Crossref | GoogleScholarGoogle Scholar |

Windig JJ, Mulder HA, ten Napel J, Knol EF, Mathur PK, Crump RE (2012) Genetic parameters for androstenone, skatole, indole, and human nose scores as measures of boar taint and their relationship with finishing traits. Journal of Animal Science 90, 2120–2129.
Genetic parameters for androstenone, skatole, indole, and human nose scores as measures of boar taint and their relationship with finishing traits.Crossref | GoogleScholarGoogle Scholar |

Zamaratskaia G, Squires EJ (2009) Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal 3, 1508–1521.
Biochemical, nutritional and genetic effects on boar taint in entire male pigs.Crossref | GoogleScholarGoogle Scholar |

Zamaratskaia G, Babol J, Andersson H, Lundström K (2004) Plasma skatole and androstenone levels in entire male pigs and relationship between boar taint compounds, sex steroids and thyroxine at various ages. Livestock Production Science 87, 91–98.
Plasma skatole and androstenone levels in entire male pigs and relationship between boar taint compounds, sex steroids and thyroxine at various ages.Crossref | GoogleScholarGoogle Scholar |