The potential of new genetic technologies in selecting for stress resistance in pigs
C. A. Kerr A B and B. M. Hines AA CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia, Qld 4067, Australia.
B Corresponding author. Email: caroline.kerr@csiro.au
Australian Journal of Experimental Agriculture 45(8) 775-782 https://doi.org/10.1071/EA05055
Submitted: 11 February 2005 Accepted: 3 June 2005 Published: 26 August 2005
Abstract
This paper examines the potential for breeding stress resistance in pigs through an understanding of the physiology of the stress response and its associated genetic basis. Pigs reared in commercial units can encounter numerous concurrent stressors that can have a negative impact on performance and welfare. Stress induces physiological and behavioural responses that are multidimensional, consisting of a complex neuroendocrine and immune signalling milieu. Some stress-related genetic parameters have been identified using conventional genetic approaches applied in experimental models. However, these traits do not capture the complexity of the stress response. As a result, the molecular mechanisms underlying the variation associated with stress resistance in pigs in a commercial environment is poorly understood. Gene expression profiling is a powerful tool that can be applied to systematically elucidate stress response pathways and networks. Consequently, gene expression technologies have been applied to identify some putative stress-regulated genes. Further application of these and more traditional technologies will aid in elucidating stress resistance using gene expression as a measure of phenotypic variation at a molecular level. It is envisaged that in the future, tools for selecting for stress resistance could eventually be applied on-farm to enhance production, health and welfare status.
Additional keywords: animal welfare, heritability, quantitative trait loci, swine.
Amuthan G,
Biswas G,
Zhang SY,
Klein-Szanto A,
Vijayasarathy C, Avadhani G
(2001) Mitochondria-to-nucleus stress signaling induces phenotypic changes, tumor progression and cell invasion. EMBO 20, 1910–1920.
| Crossref | GoogleScholarGoogle Scholar |
Baniwal SK,
Bharti K,
Chan KY,
Fauth M, Ganguli A ,
et al
.
(2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29, 471–487.
| PubMed |
Barnett JL,
Hemsworth PH,
Cronin GM,
Jongman EC, Hutson GD
(2001) A review of the welfare issues for sows and piglets in relation to housing. Australian Journal of Agricultural Research 52, 1–28.
| Crossref | GoogleScholarGoogle Scholar |
Bartolomucci A,
Palanza P,
Sacerdote P,
Panerai AE,
Sgoifo A,
Dantzer R, Parmigiani S
(2005) Social factors and individual vulnerability to chronic stress exposure. Neuroscience and Biobehavioural Reviews 29, 67–81.
| Crossref | GoogleScholarGoogle Scholar |
Bertani GR,
Gladney CD,
Johnson RK, Pomp D
(2004) Evaluation of gene expression in pigs selected for enhanced reproduction using differential display PCR. II. Anterior pituitary. Journal of Animal Science 82, 32–40.
| PubMed |
Besedovsky HO, del Rey A
(2000) The cytokine-HPA axis feed-back circuit. Zeitschrift fur Rheumatologie 59, 26–30.
Bonelli AM, Schifferli C
(2001) Porcine stress syndrome. Archivos de Medicina Veterinaria 33, 125–135.
Bornett HLI,
Morgan CA,
Lawrence AB, Mann J
(2000) The effect of group housing on feeding patterns and social behaviour of previously individually housed growing pigs. Applied Animal Behaviour Science 70, 127–141.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bronikowski AM,
Rhodes JS,
Garland T,
Prolla TA,
Award TA, Gammie SC
(2004) The evolution of gene expression in mouse hippocampus in response to selective breeding for increased locomotor activity. Evolution; International Journal of Organic Evolution 58, 2079–2086.
| PubMed |
Buitenhuis AJ,
Rodenburg TB,
Wissink PH,
Visscher J,
Koene P,
Bovenhuis H,
Ducro BJ, van der Poel JJ
(2004) Genetic and phenotypic correlations between feather pecking behavior, stress response, immune response, and egg quality traits in laying hens. Poultry Science 83, 1077–1082.
| PubMed |
Bustamante M,
Jesse GW,
Becker BA, Krause GF
(1996) Effects of individual vs group penning on performance of weanling pigs. Journal of Animal Science 74, 1457–1461.
| PubMed |
Cannon WB
(1935) Stresses and strains of homeostasis. American Journal of Medical Science 189, 1–14.
Castanon N, Mormede P
(1994) Psychobiogenetics: adapted tools for the study of the coupling between behavioural and neuroendocrine traits of emotional reactivity. Psychoneuroendocrinology 19, 257–282.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cheng HW,
Dillworth G,
Singleton P,
Chen Y, Muir WM
(2001) Effects of group selection for productivity and longevity on blood concentrations of serotonin, catecholamines, and corticosterone of laying hens Poultry Science 80, 1278–1285.
| PubMed |
Collin A,
van Milgen J,
Dubois S, Noblet J
(2001) Effect of high temperature on feeding behaviour and heat production in group-housed young pigs. The British Journal of Nutrition 8, 63–70.
Courvoisier H,
Moisan MP,
Sarrieau A,
Hendley ED, Mormede P
(1996) Behavioural and neuroendocrine reactivity to stress in the WKHA/WKY inbred rat strains: a multifactorial and genetic analysis. Brain Research 743, 77–85.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Braganca MM, Prunier A
(1999) Effects of low feed intake and hot environment on plasma profiles of glucose, nonesterified fatty acids, insulin, glucagon, and IGF-I in lactating sows. Domestic Animal Endocrinology 16, 89–101.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Groot J,
Ruis MAW,
Scholten JW,
Koolhaas JM, Boersma WJA
(2001) Long-term effects of social stress on antiviral immunity in pigs. Physiology & Behavior 73, 145–158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Haer LCM, de Vries AG
(1993) Feed intake in growing pigs. Animal Production 54, 95–104.
Desautes C,
Bidanel JP,
Milant D,
Iannuccelli N,
Amigues Y,
Bourgeois F,
Caritez JC,
Renard C,
Chevalet C, Mormede P
(2002) Genetic linkage mapping of quantitative trait loci for behavioral and neuroendocrine stress response traits in pigs. Journal of Animal Science 80, 2276–2285.
| PubMed |
Desautes C,
Bidanel JP, Mormede P
(1997) Genetic study of behavioural and pituitary–adrenocortical reactivity in response to an environmental challenge in pigs. Physiology & Behavior 62, 337–345.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Drnevich JM,
Reedy MM,
Ruedi EA,
Rodriguez-Zas S, Hughes KA
(2004) Quantitative evolutionary genomics: differential gene expression and male reproductive success in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B. Biological Sciences 271, 2267–2273.
| Crossref | GoogleScholarGoogle Scholar |
Edfors-Lilja I,
Wattrang E,
Andersson L, Fossum C
(2000) Mapping quantitative trait loci for stress induced alterations in porcine leukocyte numbers and functions. Animal Genetics 31, 186–193.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gaillard RC
(2001) Interaction between the hypothalamo–pituitary–adrenal axis and immunological system. Annales D Endocrinologie 62, 155–163.
| PubMed |
Gladney GD,
Bertani GR,
Johnson RK, Pomp D
(2004) Evaluation of gene expression in pigs selected for enhanced reproduction using differential display PCR and human microarrays. I. Ovarian follicles. Journal of Animal Science 82, 17–31.
| PubMed |
Heetkamp M,
Schrama JW,
de Jong L,
Swinkels JWGM,
Schouten WCP, Bosch MW
(1995) Energy metabolism in young pigs as affected by mixing. Journal of Animal Science 73, 3562–3569.
| PubMed |
Hicks TA,
McGlone JJ,
Whisnant CS,
Kattesh HG, Norma RL
(1998) Behavioural, endocrine, immune, and performance measures for pigs exposed to acute stress. Journal of Animal Science 76, 474–483.
| PubMed |
Hyun Y, Ellis M
(2001) Effect of group size and feeder type on growth performance and feeding patterns in growing pigs. Journal of Animal Science 79, 803–810.
| PubMed |
Hyun Y,
Ellis M, Johnson RW
(1998) Effects of feeder type, space allowance, and mixing on the growth performance and feed intake pattern of growing pigs. Journal of Animal Science 76, 2771–2778.
| PubMed |
Johnson CA
(1997) Inhibition of growth by pro-inflammatory cytokines: an integrated view. Journal of Animal Science 75, 1244–1255.
| PubMed |
Kanis E,
van den Belt H,
Groen AF,
Schakel J, de Greef KH
(2004) Breeding for improved welfare in pigs: a conceptual framework and its use in practice. Animal Science (Penicuik, Scotland) 78, 315–329.
Kerr CA,
Bunter KL,
Seymour R,
Shen B, Reverter A
(2005a) The heritability of the expression of two stress-regulated gene fragments in pigs. Journal of Animal Science 83, 1753–1765.
| PubMed |
Kerr CA,
Eamens GJ,
Briegal J,
Sheehy PA,
Giles LR, Jones MR
(2003) Effects of combined Actinobacillus pleuropneumoniae challenge and change in environmental temperature on production, plasma insulin-like growth factor I (IGF-1) and cortisol parameters in growing pigs. Australian Journal of Agricultural Research 54, 1057–1064.
| Crossref | GoogleScholarGoogle Scholar |
Kerr CA,
Giles LR,
Jones MR, Reverter A
(2005b) Effects of grouping unfamiliar cohorts, high ambient temperature and stocking density on live performance of growing pigs. Journal of Animal Science 83, 908–915.
| PubMed |
Kerr CA,
Mathews KO,
Giles LR, Jones MR
(2004) Effects of combined Actinobacillus pleuropneumoniae challenge and change in environmental temperature on calcitonin receptor expression levels in growing pigs. Australian Journal of Agricultural Research 55, 727–732.
| Crossref | GoogleScholarGoogle Scholar |
Korte SM,
Koolhaas JM,
Wingfield JC,
Wingfield JC, McEwen BS
(2005) The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews 29, 3–38.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li TH, Schmid CW
(2001) Differential stress induction of individual Alu loci: implications for transcription and retrotransposition. Gene 276, 135–141.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li TH,
Spearow J,
Rubin CM, Schmid CW
(1999) Physiological stresses increase mouse short interspersed element (SINE) RNA expression in vivo. Gene 239, 367–372.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Loeschcke V,
Sorensen JG, Kristensen TN
(2004) Ecologically relevant stress resistance: from microarrays and quantitative trait loci to candidate genes — a research plan and preliminary results using Drosophila as a model organism and climatic and genetic stress as model stresses. Journal of Biosciences 29, 503–511.
| PubMed |
Lopez J,
Jesse GW,
Becker BA, Ellersieck MR
(1991a) Effects of temperature on the performance of finishing swine. I. Effects of a hot, diurnal temperature on average daily gain, feed intake and feed efficiency. Journal of Animal Science 69, 1843–1849.
| PubMed |
Lopez J,
Jesse GW,
Becker BA, Ellersieck MR
(1991b) Effects of temperature on the performance of finishing swine. II. Effects of a cold, diurnal temperature on average daily gain, feed intake and feed efficiency. Journal of Animal Science 69, 1850–1855.
| PubMed |
Martin LB II,
Gilliam J,
Han P,
Lee K, Wikelski M
(2005) Corticosterone suppresses cutaneous immune function in temperate but not tropical House Sparrows, Passer domesticus.
General and Comparative Endocrinology 140, 126–135.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mickelson JR, Louis CF
(1996) Malignant hyperthermia: excitation–contraction coupling, Ca2+ release channel, and cell Ca2+ regulation defects. Physiological Reviews 76, 537–592.
| PubMed |
Monks SA,
Leonardson A,
Zhu H,
Cundiff P,
Pietrusiak P,
Edwards S,
Phillips JW,
Sachs A, Schadt EE
(2004) Genetic inheritance of gene expression in human cell lines. American Journal of Human Genetics 75, 1094–1105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moser RJ,
Reverter A,
Kerr CA,
Beh KJ, Lehnert SA
(2004) A mixed-model approach for the analysis of cDNA microarray gene expression data from extreme–performing pigs after infection with Actinobacillus pleuropneumoniae.
Journal of Animal Science 82, 1261–1271.
| PubMed |
Mott IW, Ivarie R
(2004) cDNA array analysis of Japanese quail lines divergently selected for four-week body weight. Poultry Science 83, 1524–1529.
| PubMed |
Muir WM, Craig JV
(1998) Improving animal well-being through genetic selection. Poultry Science 77, 1781–1788.
| PubMed |
Newman S
(1994) Quantitative-genetic and molecular–genetic effects on animal well-being–adaptive-mechanisms. Journal of Animal Science 72, 1641–1653.
| PubMed |
Nielsen BL,
Lawrence AB, Whittemore CT
(1996) Effect of individual housing on the feeding behaviour of previously group housed growing pigs. Applied Animal Behaviour Science 47, 149–161.
| Crossref | GoogleScholarGoogle Scholar |
Norry FM,
Dahlgaard J, Loeschcke V
(2004) Quantitative trait loci affecting knockdown resistance to high temperature in Drosophila melanogaster. Molecular Ecology 13, 3585–3594.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ostertag EM, Kazazian HH
(2001) Biology of mammalian L1 retrotransposons Annual Review of Genetics 35, 501–538.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pottinger TG,
Moran TA, Morgan JAW
(1994) Primary and secondary indices of stress in the progeny of rainbow trout (Oncorychus mykiss) selected for high and low responsiveness to stress. Journal of Fish Biology 44, 149–163.
| Crossref | GoogleScholarGoogle Scholar |
Ramos A,
Moisan MP,
Chaouloff F,
Mormede C, Mormede P
(1999) Identification of female-specific QTLs affecting an emotionality-related behavior in rats. Molecular Psychiatry 4, 453–462.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reichlin S
(1999) Neuroendocrinology of infection and the innate immune system. Recent Progress in Hormone Research 54, 133–181.
| PubMed |
Reif A, Lesch KP
(2003) Toward a molecular architecture of personality. Behavioural Brain Research 139, 1–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rempel WE,
Lu M,
El Kandelgy S,
Kennedy CFH,
Irvin LR,
Mickelson JR, Louis CF
(1993) Relative accuracy of the halothane challenge test and a molecular genetic test in detecting the gene for Porcine Stress Syndrome. Journal of Animal Science 71, 1395.
| PubMed |
Ritossa F
(1996) Discovery of the heat shock response. Cell Stress & Chaperones 1, 97–98.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schwerin M,
Maak S,
Hagendorf A,
von Lengerken G, Seyfert HM
(2002) A 3′-UTR variant of the inducible porcine hsp70.2 gene affects mRNA stability.
Acta — Gene Structure And Expression 1578, 90–94.
| Crossref | GoogleScholarGoogle Scholar |
Schwerin M,
Maak S,
Kalbe C, Fuerbass R
(2001) Functional promoter variants of highly conserved inducible hsp70 genes significantly affect stress response. Biochimica et Biophysica Acta 1522, 108–111.
| PubMed |
Siegel HS
(1995) Stress, strains and resistance. British Poultry Science 36, 3–22.
| PubMed |
Wallgren P,
Segall T,
Morner AP, Gunnarsson X
(1999) Experimental infections with Actinobacillus pleuropneumoniae in pigs. I. Comparison of five different parenteral antibiotic treatments. Journal of Veterinary Medicine Series B. Infectious Diseases And Veterinary Public Health 46, 249–260.
Wehrens XH,
Lehnart SE, Marks AR
(2005) Intracellular calcium release and cardiac disease. Annual Review of Physiology 67, 69–98.
| Crossref | GoogleScholarGoogle Scholar | PubMed |