Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T08:26:35.888Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of the MC4R gene on boar taint compounds, sexual maturity and behaviour in growing-finishing boars and gilts

Published online by Cambridge University Press:  09 July 2015

A. Van den Broeke ,
M. Aluwé ,
S. Janssens ,
J. Wauters ,
L. Vanhaecke ,
N. Buys ,
S. Millet  and
F. A. M. Tuyttens
A. Van den Broeke
Affiliation:
ILVO (Institute for Agricultural and Fisheries Research), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
M. Aluwé*
Affiliation:
ILVO (Institute for Agricultural and Fisheries Research), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
S. Janssens
Affiliation:
Livestock Genetics, Department of Biosystems, KU Leuven, 3001 Leuven, Belgium
J. Wauters
Affiliation:
Laboratory of Chemical Analysis, Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
L. Vanhaecke
Affiliation:
Laboratory of Chemical Analysis, Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
N. Buys
Affiliation:
Livestock Genetics, Department of Biosystems, KU Leuven, 3001 Leuven, Belgium
S. Millet
Affiliation:
ILVO (Institute for Agricultural and Fisheries Research), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
F. A. M. Tuyttens
Affiliation:
ILVO (Institute for Agricultural and Fisheries Research), Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium
*
†E-mail: [email protected]
Get access

Abstract

Societal pressure to ban surgical castration of male piglets is rising due to animal welfare concerns, thus other methods to prevent boar taint need to be explored. Genetic selection against boar taint appears to be a long-term sustainable alternative. However, as boar taint is linked to reproductive hormones, it is important to consider possible negative side effects such as delayed sexual maturity or changes in behaviour. We reported earlier that the melanocortin-4 receptor (MC4R) marker can be used to reduce boar taint levels in fat of boars. The objective of this study was to evaluate whether MC4R marker-assisted selection for lower boar taint prevalence affects plasma levels of boar taint compounds and testosterone; sexual maturity; behaviour; skin lesions; and lameness in boars and gilts. Using an intervention study with a 2×2 design, 264 boars and gilts differing on position 893 of the MC4R gene (AA v. GG) were compared. The MC4R polymorphism did not affect the plasma concentration of either androstenone or testosterone at different time points, whereas the concentration of skatole was significantly lower (P=0.003) and the concentration of indole tended to be lower (P=0.074) in GG compared with AA boars. A higher percentage of gilts of the GG genotype were in puberty at slaughter age compared with AA gilts (P<0.001). The age of the boars at sexual maturity (as indicated by the first positive preputial smear test) did not differ between AA and GG boars. In contrast, weight of GG boars at sexual maturity tended to be lower (P=0.065). During the period from 6 weeks of age to slaughter, boars and gilts of the GG genotype showed more playing behaviour (P=0.015) and less passive and feeding behaviour (P=0.003). They showed more skin lesions on their back and caudal area (P=0.022), and tended to show more skin lesions on their head and anterior area (P=0.093) compared with AA animals. In conclusion, the polymorphism in the MC4R gene can be used as a marker without negative effects on reproduction characteristics in boars and gilts. Genetic selection towards a lower prevalence of boar taint will lead to more active pigs with more skin lesions. Management strategies may therefore be necessary to reduce skin lesions in the selected animals.

Keywords

boar taintsexual maturitybehaviourpigstestosterone
Type
Research Article
Information
animal , Volume 9 , Issue 10 , October 2015 , pp. 1688 - 1697
Copyright
© The Animal Consortium 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aluwé, M, Millet, S, Nijs, G, Tuyttens, FA, Verheyden, K, Brabander, HF, Brabander, DL and Oeckel, MJ 2009. Absence of an effect of dietary fibre or clinoptilolite on boar taint in entire male pigs fed practical diets. Meat Science 82, 346–352.Google Scholar
Aluwé, M, Bekaert, KM, Tuyttens, FA, Vanhaecke, L, De, SS, De Brabander, HF, De Brabander, DL and Millet, S 2011a. Influence of soiling on boar taint in boars. Meat Science 87, 175–179.Google Scholar
Aluwé, M, Millet, S, Bekaert, KM, Tuyttens, FA, Vanhaecke, L, De, SS and De Brabander, DL 2011b. Influence of breed and slaughter weight on boar taint prevalence in entire male pigs. Animal 5, 1283–1289.CrossRefGoogle ScholarPubMed
Bagg, MA, Vassena, R, Papasso-Brambilla, E, Grupen, CG, Armstrong, DT and Gandolfi, F 2004. Changes in ovarian, follicular, and oocyte morphology immediately after the onset of puberty are not accompanied by an increase in oocyte developmental competence in the pig. Theriogenology 62, 1003–1011.CrossRefGoogle Scholar
Bekaert, KM, Vanden Bussche, J, Francois, S, Tuyttens, FA, De Brabander, HF, Vandendriessche, F and Vanhaecke, L 2012. A validated ultra-high performance liquid chromatography coupled to high resolution mass spectrometry analysis for the simultaneous quantification of the three known boar taint compounds. Journal of Chromatography A 1239, 49–55.Google Scholar
Beltranena, E, Aherne, FX, Foxcroft, GR and Kirkwood, RN 1991. Effects of pre-and postpubertal feeding on production traits at first and second estrus in gilts. Journal of Animal Science 69, 886–893.Google Scholar
Claus, R, Weiler, U and Herzog, A 1994. Physiological aspects of androstenone and skatole formation in the boar – a review with experimental data. Meat Science 38, 289–305.Google Scholar
Dorries, KM, Adkinsregan, E and Halpern, BP 1991. Sex difference in olfactory sensitivity to the boar chemosignal, androstenone, in the domestic pig. Animal Behaviour 42, 403–411.Google Scholar
Dorries, KM, Adkinsregan, E and Halpern, BP 1995. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiology and Behavior 57, 255–259.Google Scholar
Ford, JJ and Wise, TH 2011. Assessment of pubertal development of boars derived from ultrasonographic determination of testicular diameter. Theriogenology 75, 241–247.Google Scholar
Gaughan, JB, Cameron, RD, Dryden, GM and Young, BA 1997. Effect of body composition at selection on reproductive development in large white gilts. Journal of Animal Science 75, 1764–1772.Google Scholar
Gbore, FA 2009. Growth performance and puberty attainment in growing pigs fed dietary fumonisin B(1). Journal of Animal Physiology and Animal Nutrition 93, 761–767.Google Scholar
Grindflek, E, Meuwissen, THE, Aasmundstad, T, Hamland, H, Hansen, MHS, Nome, T, Kent, M, Torjesen, P and Lien, S 2011. Revealing genetic relationships between compounds affecting boar taint and reproduction in pigs. Journal of Animal Science 89, 680–692.CrossRefGoogle ScholarPubMed
Ingram, DL and Dauncey, MJ 1985. Circadian rhythms in the pig. Comparative Biochemistry and Physiology Part A: Physiology 82, 1–5.Google Scholar
Israel, DD, Sheffer-Babila, S, de Luca, C, Jo, YH, Liu, SM, Xia, Q, Spergel, DJ, Dun, SL, Dun, NJ and Chua, SC 2012. Effects of leptin and melanocortin signaling interactions on pubertal development and reproduction. Endocrinology 153, 2408–2419.Google Scholar
Kim, KS, Larsen, N, Short, T, Plastow, G and Rothschild, MF 2000. A missense variant of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth, and feed intake traits. Mammalian Genome 11, 131–135.CrossRefGoogle ScholarPubMed
Kummer, R, Bernardi, ML, Schenkel, AC, Amaral Filha, WS, Wentz, I and Bortolozzo, FP 2009. Reproductive performance of gilts with similar age but with different growth rate at the onset of puberty stimulation. Reproduction in Domestic Animals 44, 255–259.Google Scholar
McGlone, JJ and Morrow, JL 1988. Reduction of pig agonistic behavior by androstenone. Journal of Animal Science 66, 880–884.CrossRefGoogle ScholarPubMed
Mörlein, D, Lungershausen, M, Steinke, K, Sharifi, AR and Knorr, C 2012. A single nucleotide polymorphism in the CYP2E1 gene promoter affects skatole content in backfat of boars of two commercial Duroc-sired crossbred populations. Meat Science 92, 739–744.CrossRefGoogle ScholarPubMed
Nelson, AH, Mabry, JW, Benyshek, LL and Marks, MA 1990. Correlated response in reproduction, growth and composition to selection in gilts for extremes in age at puberty and backfat. Livestock Production Science 24, 237–247.CrossRefGoogle Scholar
Oskam, IC, Ropstad, E, Berg, KA, Fredriksen, B, Larsen, S, Dahl, E and Andresen, O 2008. Testicular germ cell development in relation to 5 alpha-androstenone levels in pubertal entire male pigs. Theriogenology 69, 967–976.Google Scholar
Patterson, JL, Ball, RO, Willis, HJ, Aherne, FX and Foxcroft, GR 2002. The effect of lean growth rate on puberty attainment in gilts. Journal of Animal Science 80, 1299–1310.Google Scholar
Perry, GC, Patterson, RLS, MacFie, HJH and Stinson, CG 1980. Pig courtship behaviour: pheromonal property of androstene steroids in male submaxillary secretion. Animal Production 31, 191–199.Google Scholar
R Core Team 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Rozeboom, DW, Pettigrew, JE, Moser, RL, Cornelius, SG and El Kandelgy, SM 1995. Body composition of gilts at puberty. Journal of Animal Science 73, 2524–2531.CrossRefGoogle ScholarPubMed
Rydhmer, L, Zamaratskaia, G, Andersson, HK, Algers, B, Guillemet, R and Lundstrom, K 2006. Aggressive and sexual behaviour of growing and finishing pigs reared in groups, without castration. Acta Agriculturae Scandinavica, Section A – Animal Science 56, 109–119.Google Scholar
Schroyen, M, Janssens, S, Stinckens, A, Brebels, M, Bertolini, F, Lamberigts, C, Bekaert, K, Vanhaecke, L, Aluwé, M, Tuyttens, FAM, Millet, S and Buys, N 2015. The MC4R c.893G>A mutation: a marker for growth and leanness associated with boar taint odour in Belgian pig breeds. Meat Science 101, 1–4.Google Scholar
Sellier, P and Bonneau, M 1988. Genetic relationships between fat androstenone level in males and development of male and female genital tract in pigs. Journal of Animal Breeding and Genetics 105, 11–20.Google Scholar
Strathe, AB, Velander, IH, Mark, T, Ostersen, T, Hansen, C and Kadarmideen, HN 2013. Genetic parameters for male fertility and its relationship to skatole and androstenone in Danish Landrace boars. Journal of Animal Science 91, 4659–4668.Google Scholar
Turner, SP, Farnworth, MJ, White, I, Brotherstone, S, Mendl, M, Knap, P, Penny, P and Lawrence, AB 2006. The accumulation of skin lesions and their use as a predictor of individual aggressiveness in pigs. Applied Animal Behaviour Science 96, 245–259.Google Scholar
Tuyttens, FA, Vanhonacker, F, Langendries, K, Aluwé, M, Millet, S, Bekaert, K and Verbeke, W 2011. Effect of information provisioning on attitude toward surgical castration of male piglets and alternative strategies for avoiding boar taint. Research in Veterinary Science 91, 327–332.Google Scholar
Van den Broeke, A, Aluwé, M, Tuyttens, FAM, Ampe, B, Vanhaecke, L, Wauters, J, Janssens, S, Coussé, A, Buys, N and Millet, S 2015. An intervention study demonstrates effects of MC4R genotype on boar taint and performances of growing-finishing pigs. Journal of Animal Science 93, 934–943.Google Scholar
Vandenbergh, JG 1971. The penile smear: an index of sexual maturity in male golden hamsters. Biology of Reproduction 4, 234–237.Google Scholar
Vanhonacker, F, Verbeke, W and Tuyttens, FAM 2009. Belgian consumers’ attitude towards surgical castration and immunocastration of piglets. Animal Welfare 18, 371–380.Google Scholar
Walker, WH 2010. Non-classical actions of testosterone and spermatogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 1557–1569.Google Scholar
Weiler, U, Götz, M, Schmidt, A, Otto, M and Müller, S 2013. Influence of sex and immunocastration on feed intake behavior, skatole and indole concentrations in adipose tissue of pigs. Animal 7, 300–308.Google Scholar
Wesoly, R and Weiler, U 2012. Nutritional Influences on skatole formation and skatole metabolism in the pig. Animals 2, 221–242.Google Scholar
Willeke, H, Claus, R, Muller, E, Pirchner, F and Karg, H 1987. Selection for high and low level of 5α-androst-16-en-3-one in boars. I. Direct and correlated response of endocrinologic traits. Journal of Animal Breeding and Genetics 104, 64–73.Google Scholar
Young, MG, Tokach, MD, Aherne, FX, Dritz, SS, Goodband, RD, Nelssen, JL and Loughin, TM 2008. Effect of space allowance during rearing and selection criteria on performance of gilts over three parities in a commercial swine production system. Journal of Animal Science 86, 3181–3193.Google Scholar
Zamaratskaia, G and Squires, EJ 2009. Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal 3, 1508–1521.Google Scholar
Zamaratskaia, G, Babol, J, Andersson, H and Lundstrom, 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.Google Scholar