Articles | Volume 58, issue 1
https://doi.org/10.5194/aab-58-13-2015
© Author(s) 2015. This work is distributed under
the Creative Commons Attribution 3.0 License.
the Creative Commons Attribution 3.0 License.
https://doi.org/10.5194/aab-58-13-2015
© Author(s) 2015. This work is distributed under
the Creative Commons Attribution 3.0 License.
the Creative Commons Attribution 3.0 License.
04 Mar 2015
Genetics of cattle temperament and its impact on livestock production and breeding – a review
J. Friedrich
Institute of Animal Science and Technology, University of Rostock, Rostock, Germany
B. Brand
Institute for Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
M. Schwerin
CORRESPONDING AUTHOR
Institute of Animal Science and Technology, University of Rostock, Rostock, Germany
Institute for Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
Cited articles
Abrial, E., Etievant, A., Bétry, C., Scarna, H., Lucas, G., Haddjeri, N., and Lambás-Señas, L.: Protein kinase C regulates mood-related behaviors and adult hippocampal cell proliferation in rats, Prog. Neuropsychoph., 43, 40–48, 2013.
Adamczyk, K., Pokorska, J., Makulska, J., Earley, B., and Mazurek, M.: Genetic analysis and evaluation of behavioural traits in cattle, Livest. Sci., 154, 1–12, 2013.
Bailey, J. N., Breidenthal, S. E., Jorgensen, M. J., McCracken, J. T., and Fairbanks, L. A.: The association of DRD4 and novelty seeking is found in a nonhuman primate model, Psychiat. Genet., 17, 23–27, 2007.
Baker, B. S., Taylor, B. J., and Hall, J. C.: Are Complex Behaviors Specified by Dedicated Regulatory Genes? Reasoning from Drosophila, Cell, 105, 13–24, 2001.
Bartussek, H., Leeb, C., and Held, S.: Animal needs index for cattle. ANI 35L/2000-cattle, Federal Research Institute for Agriculture in Alpine Regions BAL Gumpenstein, Irdning, Austria, 2000.
Bendesky, A. and Bargmann, C. I.: Genetic contributions to behavioural diversity at the gene-environment interface, Nat. Rev. Genet., 12, 809–820, 2011.
Benhajali, H., Boivin, X., Sapa, J., Pellegrini, P., Boulesteix, P., Lajudie, P., and Phocas, F.: Assessment of different on-farm measures of beef cattle temperament for use in genetic evaluation, J. Anim. Sci., 88, 3529–3537, 2010.
Black, T. E., Bischoff, K. M., Mercadante, V. R. G., Marquezini, G. H. L., DiLorenzo, N., Chase Jr., C. C., Coleman, S. W., Maddock, T. D., and Lamb, G. C.: Relationships among performance, residual feed intake, and temperament assessed in growing beef heifers and subsequently as 3-year-old, lactating beef cows, J. Anim. Sci., 91, 2254–2263, 2013.
Bøe, K. E. and Færevik, G.: Grouping and social preferences in calves, heifers and cows, Appl. Anim. Behav. Sci., 80, 175–190, 2003.
Boissy, A., Fisher, A. D., Bouix, J., Hinch, G. N., and Le Neindre, P.: Genetics of fear in ruminant livestock, Livest. Prod. Sci., 93, 23–32, 2005.
Boivin, X., Le Neindre, P., Chupin, J. M., Garel, J. P., and Trillat, G.: Influence of breed and early management on ease of handling and open-field behaviour of cattle, Appl. Anim. Behav. Sci., 32, 313–323, 1992.
Boldt, C. R.: A study of cattle disposition: Exploring QTL associated with temperament, Senior honors thesis, Texas A&M University, College Station, TX, USA, 2008.
Breuer, K., Hemsworth, P. H., Barnett, J. L., Matthews, L. R., and Coleman, G. J.: Behavioural response to humans and the productivity of commercial dairy cows, Appl. Anim. Behav. Sci., 66, 273–288, 2000.
Broom, D. M.: Indicators of poor welfare, Br. Vet. J., 142, 524–526, 1986.
Brouček, J., Uhriniča\vt, M., Šoch, M., and Kišac, P.: Genetics of behaviour in cattle, Slovak. J. Anim. Sci., 41, 166–172, 2008.
Bruckmaier, R. M. and Blum, J. W.: Oxytocin Release and Milk Removal in Ruminants, J. Dairy Sci., 81, 939–949, 1998.
Burdick, N. C., Carroll, J. A., Hulbert, L. E., Dailey, J. W., Willard, S. T., Vann, R. C., Welsh Jr., T. H., and Randel, R. D.: Relationships between temperament and transportation with rectal temperature and serum concentrations of cortisol and epinephrine in bulls, Livest. Sci., 129, 166–172, 2010.
Burdick, N. C., Randel, R. D., Carroll, J. A., and Welsh Jr., T. H.: Interactions between Temperament, Stress, and Immune Funtion in Cattle, Int. J. Zool., 2011, Article ID 373197, 9 pages, 2011.
Burrow, H. M.: Measurements of temperament and their relationships with performance traits of beef cattle, Anim. Breed. Abstr., 65, 477–495, 1997.
Burrow, H. M.: Variances and covariances between productive and adaptive traits and temperament in a composite breed of tropical beef cattle, Livest. Prod. Sci., 70, 213–233, 2001.
Cafe, L. M., Robinson, D. L., Ferguson, D. M., Geesink, G. H., and Greenwood, P. L.: Temperament and hypothalamic-pituitary-adrenal axis function are related and combine to affect growth, efficiency, carcass, and meat quality traits in Brahman steers, Domest. Anim. Endocrinol., 40, 230–240, 2011a.
Cafe, L. M., Robinson, D. L., Ferguson, D. M., McIntyre, B. L., Geesink, G. H., and Greenwood, P. L.: Cattle temperament: Persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits, J. Anim. Sci, 89, 1452–1465, 2011b.
Canario, L., Mignon-Grasteau, S., Dupont-Nivet, M., and Phocas, F.: Genetics of behavioural adaptation of livestock to farming conditions, Animal, 7, 357–377, 2013.
Cooke, R. F., Bohnert, D. W., Meneghetti, M., Losi, T. C., and Vasconcelos, J. L. M.: Effects of temperament on pregnancy rates to fixed-time AI in Bos indicus beef cows, Livest. Sci., 142, 108–113, 2011.
Core, S., Widowski, T., Mason, G., and Miller, S.: Eye white percentage as a predictor of temperament in beef cattle, J. Anim. Sci., 87, 2168–2174, 2009.
Curley Jr., K. O., Neuendorff, D. A., Lewis, A. W., Cleere, J. J., Welsh Jr., T. H., and Randel, R. D.: Functional characteristics of the bovine hypothalamic-pituitary-adrenal axis vary with temperament, Horm. Behav., 53, 20–27, 2008.
Cyr, N. E. and Romero, L. M.: Identifying hormonal habituation in field studies of stress, Gen. Comp. Endocrinol., 161, 295–303, 2009.
Dickson, D. P., Barr, G. R., Johnson, L. P., and Wieckert, D. A.: Social Dominance and Temperament in Holstein Cows, J. Dairy. Sci., 53, 904–907, 1970.
FAWC: Press statement from the Farm Animal Welfare Council, http://webarchive.nationalarchives.gov.uk/20121007104210/http://www.fawc.org.uk/pdf/fivefreedoms1979.pdf (last access: 15 November 2014), 1979.
Ferguson, D. M. and Warner, R. D.: Have we underestimated the impact of pre-slaughter stress on meat quality in ruminants?, Meat. Sci., 80, 12–19, 2008.
Fisher, A. D., Morris, C. A., Matthews, L. R., Pitchford, W. S., and Bottema, C. D. K.: Handling and stress response traits in cattle: identification of putative genetic markers, in: Proc 35th Intern Conf ISAE, University of Ccalifornia Davis, Davis, CA, USA, p. 100, 2001.
Flint, J.: Analysis of quantitative trait loci that influence animal behavior, J. Neurobiol., 54, 46–77, 2003.
Flisikowski, K., Schwarzenbacher, H., Wysocki, M., Weigend, S., Preisinger, R., Kjaer, J. B., and Fries, R.: Variation in neighbouring genes of the dopaminergic and serotonergic systems affects feather pecking behaviour of laying hens, Anim. Genet., 40, 192–199, 2009.
Gauly, M., Mathiak, H., Hoffmann, K., Kraus, M., and Erhardt, G.: Estimating genetic variability in temperamental traits in German Angus and Simmental cattle, Appl. Anim. Behav. Sci., 74, 109–119, 2001.
Gauly, M., Mathiak, H., and Erhardt, G.: Genetic background of behavioural and plasma cortisol response to repeated short-term separation and tethering of beef calves, J. Anim. Breed. Genet., 119, 379–384, 2002.
Gibbons, J., Lawrence, A., and Haskell, M.: Responsiveness of dairy cows to human approach and novel stimuli, Appl. Anim. Behav. Sci., 116, 163–173, 2009.
Gibbons, J. M., Lawrence, A. B., and Haskell, M. J.: Consistency of flight speed and response to restraint in a crush in dairy cattle, Appl. Anim. Behav. Sci., 131, 15–20, 2011.
Glenske, K., Prinzenberg, E. M., Brandt, H., Gauly, M., and Erhardt, G.: A chromosome-wide QTL study on BTA29 affecting temperament traits in German Angus beef cattle and mapping of DRD4, Animal, 5, 195–197, 2011.
Grandin, T.: Solving livestock handling problems, Vet. Med., 89, 989–998, 1994.
Grandin, T. and Dessing, M. J.: Behavioral genetics and animal science, in: Genetics and the behavior of domestic animals, edited by: Grandin, T., Academic Press, San Diego, CA, USA, 1–30, 1998.
Grignard, L., Boivin, X., Boissy, A., and Le Neindre, P.: Do beef cattle react consistently to different handling situations?, Appl. Anim. Behav. Sci., 71, 263–276, 2001.
Gutiérrez-Gil, B., Ball, N., Burton, D., Haskell, M., Williams, J. L., and Wiener, P.: Identification of Quantitative Trait Loci Affecting Cattle Temperament, J. Hered., 99, 629–638, 2008.
Hall, N. L., Buchanan, D. S., Anderson, V. L., Ilse, B. R., Carlin, K. R., and Berg, E. P.: Working chute behavior of feedlot cattle can be an indication of cattle temperament and beef carcass composition and quality, Meat. Sci., 89, 52–57, 2011.
Hasegawa, T.: Tyrosinase-Expressing Neuronal Cell Line as in Vitro Model of Parkinson's Disease, Int. J. Mol. Sci., 11, 1082–1089, 2010.
Haskell, M. J., Bell, D. J., and Gibbons, J. M.: Is the response to humans consistent over productive life in dairy cows?, Anim. Welfare, 21, 319–324, 2012.
Hemsworth, P. H., Coleman, G. J., Barnett, J. L., and Borg, S.: Relationships between human-animal interactions and productivity of commercial dairy cows, J. Anim. Sci., 78, 2821–2831, 2000.
Hiendleder, S., Thomsen, H., Reinsch, N., Bennewitz, J., Leyhe-Horn, B., Looft, C., Xu, N., Medjugorac, I., Russ, I., Kühn, C., Brockmann, G. A., Blümel, J., Brenig, B., Reinhardt, F., Reents, R., Averdunk, G., Schwerin, M., Förster, M., Kalm, E., and Erhardt, G.: Mapping of QTL for Body Conformation and Behavior in Cattle, J. Hered., 94, 496–506, 2003.
Hoppe, S., Brandt, H. R., König, S., Erhardt, G., and Gauly, M.: Temperament traits of beef calves measured under field conditions and their relationships to performance, J. Anim. Sci., 88, 1982–1989, 2010.
Hopster, H.: Coping strategies in dairy cows, Doctoral thesis, Agricultural University Wageningen, Wageningen, Netherlands, 1998.
Hulsegge, I., Woelders, H., Smits, M., Schokker, D., Jiang, L., and Sørensen, P.: Prioritization of candidate genes for cattle reproductive traits, based on protein-protein interactions, gene expression, and text-mining, Physiol. Genomics, 45, 400–406, 2013.
Jensen, P.: Domestication – From behaviour to genes and back again, Appl. Anim. Behav. Sci., 97, 3–15, 2006.
Johnston, T. D. and Edwards, L.: Genes, interactions, and the development of behavior, Psychol. Rev., 109, 26–34, 2002.
Kilgour, R.: The open-field test as an assessment of the temperament of dairy cows, Anim. Behav., 23, 615–624, 1975.
King, D. A., Schuehle Pfeiffer, C. E., Randel, R. D., Welsh Jr., T. H., Oliphint, R. A., Baird, B. E., Curley Jr., K. O., Vann, R. C., Hale, D. S., and Savell, J. W.: Influence of animal temperament and stress responsiveness on the carcass quality and beef tenderness of feedlot cattle, Meat. Sci., 74, 546–556, 2006.
Kommadath, A., Woelders, H., Beerda, B., Mulder, H. A., de Wit, A. A. C., Veerkamp, R. F., te Pas, M. F. W., and Smits, M. A.: Gene expression patterns in four brain areas associate with quantitative measure of estrous behavior in dairy cows, BMC Genomics, 12, 200, 2011.
König, S., Köhn, F., Kuwan, K., Simianer, H., and Gauly, M.: Use of Repeated Measures Analysis for Evaluation of Genetic Background of Dairy Cattle Behavior in Automatic Milking Systems, J. Dairy Sci., 89, 3636–3644, 2006.
Korsten, P., Mueller, J. C., Hermannstädter, C., Bouwman, K. M., Dingemanse, N. J., Drent, P. J., Liedvogel, M., Matthysen, E., van Oers, K., van Overveld, T., Patrick, S. C., Quinn, J. L., Sheldon, B. C., Tinbergen, J. M., and Kempenaers, B.: Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations, Mol. Ecol., 19, 832–843, 2010.
Lanier, J. L., Grandin, T., Green, R. D., Avery, D., and McGee, K.: The relationship between reaction to sudden, intermittent movements and sounds and temperament, J. Anim. Sci., 78, 1467–1474, 2000.
Lawstuen, D. A., Hansen, L. B., and Steuernagel, G. R.: Management Traits Scored Linearly by Dairy Producers, J. Dairy Sci., 71, 788–799, 1988.
Le Neindre, P., Boivin, X., and Boissy, A.: Handling of extensively kept animals, Appl. Anim. Behav. Sci., 49, 73–81, 1996.
Lühken, G., Glenske, K., Brandt, H., and Erhardt, G.: Genetic variation in monoamine oxidase A and analysis of association with behaviour traits in beef cattle, J. Anim. Breed. Genet., 127, 411–418, 2010.
Magolski, J. D., Berg, E. P., Hall, N. L., Anderson, V. L., Keller, W. L., Jeske, T. M., and Maddock Carlin, K. R.: Evaluation of feedlot cattle working chute behavior relative to temperament, tenderness, and postmortem proteolysis, Meat. Sci., 95, 92–97, 2013.
Mazurek, M., McGee, M., Crowe, M. A., Prendiville, D. J., Boivin, X., and Earley, B.: Consistency and stability of behavioural fear responses of heifers to different fear-eliciting situations involving humans, Appl. Anim. Behav. Sci., 131, 21–28, 2011.
Mormède, P.: Molecular genetics of behaviour: research strategies and perspectives for animal production, Livest. Prod. Sci., 93, 15–21, 2005.
Morris, C. A., Cullen, N. G., Kilgour, R., and Bremner, K. J.: Some genetic factors affecting temperament in Bos taurus cattle, New Zeal. J. Agr. Res., 37, 167–175, 1994.
Munafò, M. R., Yalcin, B., Willis-Owen, S. A., and Flint, J.: Association of the Dopamine D4 Receptor (DRD4) Gene and Approach-Related Personality Traits: Meta-Analysis and New Data, Biol. Psychiat., 63, 197–206, 2008.
Muráni, E., Ponsuksili, S., D'Eath, R. B., Turner, S. P., Kurt, E., Evans, G., Thölking, L., Klont, R., Foury, A., Mormède, P., and Wimmers, K.: Association of HPA axis-related genetic variation with stress reactivity and aggressive behaviour in pigs, BMC Genetics, 11, 74, 2010.
Murphey, R. M., Moura Duarte, F. A., Torres Penedo, M. C.: Approachability of Bovine Cattle in Pastures: Breed Comparisons and a Breed x Treatment Analysis, Behav. Genet., 10, 171–181, 1980.
Nkrumah, J. D., Li, C., Yu, J., Hansen, C., Keisler, D. H., and Moore, S. S.: Polymorphisms in the bovine leptin promoter associated with serum leptin concentration, growth, feed intake, feeding behavior, and measures of carcass merit, J. Anim. Sci., 83, 20–28, 2005.
Nkrumah, J. D., Crews Jr., D. H., Basarab, J. A., Price, M. A., Okine, E. K., Wang, Z., Li, C., and Moore, S. S.: Genetic and phenotypic relationships of feeding behavior and temperament with performance, feed efficiency, ultrasound, and carcass merit of beef cattle, J. Anim. Sci., 85, 2382–2390, 2007.
Oltenacu, P. A. and Broom, D. M.: The impact of genetic selection for increased milk yield on the welfare of dairy cows, Anim. Welfare, 19, 39–49, 2010.
Orbán, M., Gaál, K. K., Pajor, F., Szentléleki, A., Póti, P., Tözsér, J., and Gulyás, L.: Effect of temperament of Jersey and Holstein Friesian cows on milk production traits and somatic cell count, Arch. Tierz., 54, 594–599, 2011.
Petherick, J. C., Holroyd, R. G., Doogan, V. J., and Venus, B. K.: Productivity, carcass and meat quality of lot-fed Bos indicus cross steers grouped according to temperament, Aust. J. Exp. Agric., 42, 389–398, 2002.
Phocas, F., Boivin, X., Sapa, J., Trillat, G., Boissy, A., and Le Neindre, P.: Genetic correlations between temperament and breeding traits in Limousin heifers, Anim. Sci., 82, 805–811, 2006.
Price, E. O.: Behavioral development in animals undergoing domestication, Appl. Anim. Behav. Sci., 65, 245–271, 1999.
Price, E. O.: Neurophysiological approaches to the study of behavior genetics, in: Principles and applications of domestic animal behavior, edited by: Price, E. O., CABI, Wallingfort et al., UK, 21–22, 2008.
Raussi, S.: Human-cattle interactions in group housing, Appl. Anim. Behav. Sci., 80, 245–262, 2003.
Réale, D., Reader, S. M., Sol, D., McDougall, P. T., and Dingemanse, N. J.: Integrating animal temperament within ecology and evolution, Biol. Rev., 82, 291–318, 2007.
Reaume, C. J. and Sokolowski, M. B.: cGMP-Dependent Protein Kinase as a Modifier of Behaviour, Handbook of Experimental Pharmacology, 191, 423–443, 2009.
Reiner, G., Köhler, F., Berge, T., Fischer, R., Hübner-Weitz, K., Scholl, J., and Willems, H.: Mapping of quantitative trait loci affecting behaviour in swine, Anim. Genet., 40, 366–376, 2009.
Rupp, R. and Boichard, D.: Genetic Parameters for Clinical Mastitis, Somatic Cell Score, Production, Udder Type Traits, and Milking Ease in First Lactation Holsteins, J. Dairy Sci., 82, 2198–2204, 1999.
Rushen, J., Munksgaard, L., Marnet, P. G., and DePassillé, A. M.: Human contact and the effects of acute stress on cows at milking, Appl. Anim. Behav. Sci., 73, 1–14, 2001.
Sant'Anna, A. C., Paranhos da Costa, M. J. R., Baldi, F., and Albuquerque, L. G.: Genetic variability for temperament indicators of Nellore cattle, J. Anim. Sci., 91, 3532–3537, 2013.
Schmidtz, B. H., Buchanan, F. C., Plante, Y., and Schmutz, S. M.: Linkage mapping of the tyrosinase gene to bovine chromosome 29, Anim. Genet., 32, 119–120, 2001.
Schmutz, S. M., Stookey, J. M., Winkelman-Sim, D. C., Waltz, C. S., Plante, Y., and Buchanan, F. C.: A QTL Study of Cattle Behavioral Traits in Embryo Transfer Families, J. Hered., 92, 290–292, 2001.
Schrooten, C., Bovenhuis, H., Coppieters, W., and Van Arendonk, J. A. M.: Whole Genome Scan to Detect Quantitative Trait Loci for Conformation and Functional Traits in Dairy Cattle, J. Dairy Sci., 83, 795–806, 2000.
Schütz, K. E., Hawke, M., Waas, J. R., McLeay, L. M., Bokkers, E. A. M., van Reenen, C. G., Webster, J. R., and Stewart, M.: Effects of human handling during early rearing on the behaviour of dairy calves, Anim. Welfare, 21, 19–26, 2012.
Schwartzkopf-Genswein, K. S., Shah, M. A., Church, J. S., Haley, D. B., Janzen, K., Truong, G., Atkins, R. P., and Crowe, T. G.: A comparison of commonly used and novel electronic techniques for evaluating cattle temperament, Can. J. Anim. Sci., 92, 21–31, 2012.
Sewalem, A., Miglior, F., and Kistemaker, G. J.: Short communication: Genetic parameters of milking temperament and milking speed in Canadian Holsteins, J. Dairy Sci., 94, 512–516, 2011.
Shih, J. C., Chen, K., and Ridd, M. J.: Monoamine oxidase: From genes to behavior, Annu. Rev. Neurosci., 22, 197–217, 1999.
Spelman, R. J., Huisman, A. E., Singireddy, S. R., Coppieters, R. J., Arranz, J., Georges, M., and Garrick, D. J.: Quantitative Trait Loci Analysis on 17 Nonproduction Traits in the New Zealand Dairy Population, J. Dairy Sci., 82, 2514–2516, 1999.
Sutherland, M. A., Rogers, A. R., and Verkerk, G. A.: The effect of temperament and responsiveness towards humans on the behavior, physiology and milk production of multi-parous dairy cows in a familiar and novel milking environment, Physiol. Behav., 107, 329–337, 2012.
Van Reenen, C. G., Van der Werf, J. T. N., Bruckmaier, R. M., Hopster, H., Engel, B., Noordhuizen, J. P. T. M., and Blokhuis, H. J.: Individual Differences in Behavioral and Physiological Responsiveness of Primiparous Dairy Cows to Machine Milking, J. Dairy Sci., 85, 2551–2561, 2002.
Veissier, I., Aubert, A., and Boissy, A.: Animal welfare: A result of animal background and perception of its environment, Anim. Front., 2, 7–15, 2012.
Vetters, M. D. D., Engle, T. E., Ahola, J. K., and Grandin, T.: Comparison of flight speed and exit score as measurements of temperament in beef cattle, J. Anim. Sci., 91, 374–381, 2013.
Visscher, P. M. and Goddard, M. E.: Genetic Parameters for Milk Yield, Survival, Workability, and Type Traits for Australian Dairy Cattle, J. Dairy Sci., 78, 205–220, 1995.
Voisinet, B. D., Grandin, T., Tatum, J. D., O'Connor, S. F., and Struthers, J. J.: Feedlot cattle with calm temperaments have higher average daily gains than cattle with excitable temperaments, J. Anim. Sci., 75, 892–896, 1997.
Von Keyserlingk, M. A. G., Rushen, J., de Passillé, A. M., and Weary, D. M.: Invited review: The welfare of dairy cattle–Key concepts and the role of science, J. Dairy Sci., 92, 4101–4111, 2009.
Waiblinger, S., Menke, C., and Fölsch, D. W.: Influences on the avoidance and approach behaviour of dairy cows towards humans on 35 farms, Appl. Anim. Behav. Sci., 84, 23–39, 2003.
Watts, J. M., Stookey, J. M., Schmutz, S. M., and Waltz, C. S.: Variability in vocal and behavioural responses to visual isolation between full-sibling families of beef calves, Appl. Anim. Behav. Sci., 70, 255–273, 2001.
Wegenhoft, M. A.: Locating quantitative trait loci associated with disposition in cattle, Senior honors thesis, Texas A&M University, College Station, TX, USA, 2005.
Welfare Quality®: Welfare Quality® assessment protocol for cattle, Welfare Quality® Consortium, Lelystad, Netherlands, 2009.
