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Genome-wide associations for feed utilisation complex in primiparous Holstein–Friesian dairy cows from experimental research herds in four European countries

  • R. F. Veerkamp (a1), M. P. Coffey (a2), D. P. Berry (a3), Y. de Haas (a1), E. Strandberg (a4), H. Bovenhuis (a5), M. P. L. Calus (a1) and E. Wall (a2)...


Genome-wide association studies for difficult-to-measure traits are generally limited by the sample size with accurate phenotypic data. The objective of this study was to utilise data on primiparous Holstein–Friesian cows from experimental farms in Ireland, the United Kingdom, the Netherlands and Sweden to identify genomic regions associated with the feed utilisation complex: fat and protein corrected milk yield (FPCM), dry matter intake (DMI), body condition score (BCS) and live-weight (LW). Phenotypic data and 37 590 single nucleotide polymorphisms (SNPs) were available on up to 1629 animals. Genetic parameters of the traits were estimated using a linear animal model with pedigree information, and univariate genome-wide association analyses were undertaken using Bayesian stochastic search variable selection performed using Gibbs sampling. The variation in the phenotypes explained by the SNPs on each chromosome was related to the size of the chromosome and was relatively consistent for each trait with the possible exceptions of BTA4 for BCS, BTA7, BTA13, BTA14, BTA18 for LW and BTA27 for DMI. For LW, BCS, DMI and FPCM, 266, 178, 206 and 254 SNPs had a Bayes factor >3, respectively. Olfactory genes and genes involved in the sensory smell process were overrepresented in a 500 kbp window around the significant SNPs. Potential candidate genes were involved with functions linked to insulin, epidermal growth factor and tryptophan.


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Banos, G, Brotherstone, S, Coffey, MP 2004. Evaluation of body condition score measured throughout lactation as an indicator of fertility in dairy cattle. Journal of Dairy Science 87, 26692676.
Banos, G, Woolliams, JA, Woodward, BW, Forbes, AB, Coffey, MP 2008. Impact of single nucleotide polymorphisms in leptin, leptin receptor, growth hormone receptor, and diacylglycerol acyltransferase (DGAT1) gene loci on milk production, feed, and body energy traits of UK dairy cows. Journal of Dairy Science 91, 31903200.
Banos, G, Coffey, MP, Veerkamp, RF, Berry, DP, Wall, E 2012. Merging and characterising phenotypic data on conventional and rare traits from dairy cattle experimental resources in three countries. Animal 6, 10401048.
Beerda, B, Ouweltjes, W, Sebek, LBJ, Windig, JJ, Veerkamp, RF 2007. Effects of genotype by environment interactions on milk yield, energy balance, and protein balance. Journal of Dairy Science 90, 219228.
Berry, DP, Buckley, F, Dillon, P, Evans, RD, Rath, M, Veerkamp, RF 2002. Genetic parameters for level and change of body condition score and body weight in dairy cows. Journal of Dairy Science 85, 20302039.
Berry, DP, Buckley, F, Dillon, P, Evans, RD, Rath, M, Veerkamp, RF 2003. Genetic parameters for body condition score, body weight, milk yield, and fertility estimated using random regression models. Journal of Dairy Science 86, 37043717.
Berry, DP, Horan, B, O'Donovan, M, Buckley, F, Kennedy, E, McEvoy, M, Dillon, P 2007. Genetics of grass dry matter intake, energy balance, and digestibility in grazing Irish dairy cows. Journal of Dairy Science 90, 48354845.
Browning, SR, Browning, BL 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. American Journal of Human Genetics 81, 10841097.
Calus, MPL, Veerkamp, RF 2011. Accuracy of multi-trait genomic selection using different methods. Genetic Selection Evolution 43, 2640.
Calus, MPL, Mulder, HA, Bastiaansen, JWM 2011. Identification of Mendelian inconsistencies between SNP and pedigree information of sibs. Genetics Selection Evolution 43, 3446.
Campbell, ID, Baron, M, Cooke, RM, Dudgeon, TJ, Fallon, A, Harvey, TS, Tappin, MJ 1990. Structure–function-relationships in epidermal growth-factor (EGF) and transforming growth factor-alpha (TGF-ALPHA). Biochemical Pharmacology 40, 3540.
Choung, JJ, Chamberlain, DG 1992. Protein nutrition of dairy-cows receiving grass-silage diets – effects on silage intake and milk-production of postruminal supplements of casein or soya-protein isolate and the effects of intravenous infusions of a mixture of methionine, phenylalanine and tryptophan. Journal of the Science of Food and Agriculture 58, 307314.
Coffey, MP, Simm, G, Hill, WG, Brotherstone, S 2003. Genetic evaluations of dairy bulls for daughter energy balance profiles using linear type scores and body condition score analyzed using random regression. Journal of Dairy Science 86, 22052212.
Coffey, MP, Simm, G, Oldham, JD, Hill, WG, Brotherstone, S 2004. Genotype and diet effects on energy balance in the first three lactations of dairy cows. Journal of Dairy Science 87, 43184326.
Coskun, S, Ozer, C, Gonul, B, Take, G, Erdogan, D 2006. The effect of repeated tryptophan administration on body weight, food intake, brain lipid peroxidation and serotonin immunoreactivity in mice. Molecular and Cellular Biochemistry 286, 133138.
Daetwyler, HD 2009. Genome-wide evaluation of populations. Wageningen University, Wageningen, The Netherlands.
Dal Zotto, R, De Marchi, M, Dalvit, C, Cassandro, M, Gallo, L, Carnier, P, Bittante, G 2007. Heritabilities and genetic correlations of body condition score and calving interval with yield, somatic cell score, and linear type traits in Brown Swiss cattle. Journal of Dairy Science 90, 57375743.
de Roos, APW, Hayes, BJ, Spelman, RJ, Goddard, ME 2008. Linkage disequilibrium and persistence of phase in Holstein–Friesian, Jersey and Angus cattle. Genetics 179, 15031512.
Dillon, P, Berry, DP, Evans, RD, Buckley, F, Horan, B 2006. Consequences of genetic selection for increased milk production in European seasonal pasture based systems of milk production. Livestock Science 99, 141158.
Fuller, TF, Ghazalpour, A, Aten, JE, Drake, TA, Lusis, AJ, Horvath, S 2007. Weighted gene coexpression network analysis strategies applied to mouse weight. Mammalian Genome 18, 463472.
Gauthier, BR, Wollheim, CB 2008. Synaptotagmins bind calcium to release insulin. American Journal of Physiology – Endocrinology and Metabolism 295, E1279E1286.
Gilmour, AR, Cullis, BR, Welham, SJ, Thompson, R 2009. ASREML. Program user manual. NSW Agriculture, Orange Agricultural Institute, Orange, NSW, Australia.
Haider, S, Ballester, B, Smedley, D, Zhang, JJ, Rice, P, Kasprzyk, A 2009. BioMart Central Portal – unified access to biological data. Nucleic Acids Research 37, W23W27.
Hill, WG, Robertson, A 1986. Linkage disequilibrium in finite populations. Theoretical and Applied Genetics 38, 226231.
Horan, B, Dillon, P, Berry, DP, O'Connor, P, Rath, M 2005. The effect of strain of Holstein–Friesian, feeding system and parity on lactation curves characteristics of spring-calving dairy cows. Livestock Production Science 95, 231241.
Huang, DW, Sherman, BT, Lempicki, RA 2009a. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4, 4457.
Huang, DW, Sherman, BT, Lempicki, RA 2009b. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37, 113.
Kass, RE, Raftery, AE 1995. Bayes factors. Journal of the American Statistical Association 90, 773795.
Koenen, EPC, Veerkamp, RF 1998. Genetic covariance functions for live weight, condition score, and dry-matter intake measured at different lactation stages of Holstein Friesian heifers. Livestock Production Science 57, 6777.
Koenen, EPC, Veerkamp, RF, Dobbelaar, P, De Jong, G 2001. Genetic analysis of body condition score of lactating Dutch Holstein and Red-and-White heifers. Journal of Dairy Science 84, 12651270.
Koopmans, SJ, Guzik, AC, van der Meulen, J, Dekker, R, Kogut, J, Kerr, BJ, Southern, LL 2006. Effects of supplemental l-tryptophan on serotonin, cortisol, intestinal integrity, and behavior in weanling piglets. Journal of Animal Science 84, 963971.
Liefers, SC, te Pas, MFW, Veerkamp, RF, van der Lende, T 2002. Associations between leptin gene polymorphisms and production, live weight, energy balance, feed intake, and fertility in Holstein heifers. Journal of Dairy Science 85, 16331638.
Liefers, SC, Veerkamp, RF, Pas, M, Delavaud, C, Chilliard, Y, Platje, M, van der Lende, T 2005. Leptin promoter mutations affect leptin levels and performance traits in dairy cows. Animal Genetics 36, 111118.
Macciotta, NPP, Mele, M, Conte, G, Serra, A, Cassandro, M, Dal Zotto, R, Borlino, AC, Pagnacco, G, Secchiari, P 2008. Association between a polymorphism at the stearoyl CoA desaturase locus and milk production traits in Italian Holsteins. Journal of Dairy Science 91, 31843189.
MacNeil, MD, Grosz, MD 2002. Genome-wide scans for QTL affecting carcass traits in Hereford × composite double backcross populations. Journal of Animal Science 80, 23162324.
Meuwissen, THE, Goddard, ME 2004. Mapping multiple QTL using linkage disequilibrium and linkage analysis information and multitrait data. Genetics Selection Evolution 36, 261279.
Montgomery, GW, Flux, DS, Greenway, RM 1980. Tryptophan deficiency in pigs – changes in food-intake and plasma-levels of glucose, amino-acids, insulin and growth-hormone. Hormone and Metabolic Research 12, 304309.
Mullen, MP, Berry, DP, Howard, DJ, Diskin, MG, Lynch, CO, Berkowicz, EW, Magee, DA, MacHugh, DE, Waters, SM 2010. Associations between novel single nucleotide polymorphisms in the Bos taurus growth hormone gene and performance traits in Holstein–Friesian dairy cattle. Journal of Dairy Science 93, 59595969.
Oikonomou, G, Angelopoulou, K, Arsenos, G, Zygoyiannis, D, Banos, G 2009. The effects of polymorphisms in the DGAT1, leptin and growth hormone receptor gene loci on body energy, blood metabolic and reproductive traits of Holstein cows. Animal Genetics 40, 1017.
Petersson, KJ, Strandberg, E, Gustafsson, H, Berglund, B 2006. Environmental effects on progesterone profile measures of dairy cow fertility. Animal Reproduction Science 91, 201214.
Pryce, JE, Nielsen, BL, Veerkamp, RF, Simm, G 1999. Genotype and feeding system effects and interactions for health and fertility traits in dairy cattle. Livestock Production Science 57, 193201.
Seidenspinner, T, Tetens, J, Habier, D, Bennewitz, J, Thaller, G 2011. The placental growth factor (PGF) – a positional and functional candidate gene influencing calving ease and stillbirth in German dairy cattle. Animal Genetics 42, 2227.
Sheehy, PA, Riley, LG, Raadsma, HW, Williamson, P, Wynn, PC 2009. A functional genomics approach to evaluate candidate genes located in a QTL interval for milk production traits on BTA6. Animal Genetics 40, 492498.
Sved, JA 1971. Linkage disequilibrium and homozygosity of chromosome segments in finite populations. Theoretical Population Biology 2, 125141.
Svendsen, M, Skipenes, P, Mao, IL 1994. Genetic correlations in the feed conversion complex of primiparous cows at a recommended and a reduced plane of nutrition. Journal of Animal Science 72, 14411449.
Van der Lende, T, Te Pas, MFW, Veerkamp, RF, Liefers, SC 2005. Leptin gene polymorphisms and their phenotypic associations. In Vitamins and hormones – advances in research and applications (ed. Gerald Litwack), vol. 71, pp. 373–404. Elsevier Academic press, San Diego, California, USA
Veerkamp, RF 1998. Selection for economic efficiency of dairy cattle using information on live weight and feed intake: a review. Journal of Dairy Science 81, 11091119.
Veerkamp, RF 2002. Feed intake and energy balance in lactating animals. In Proceedings of the 7th World Congress on Genetics Applied to Livestock Production, Montpellier, France, CD-ROM Session 10-01.
Veerkamp, RF, Simm, G, Oldham, JD 1995. Genotype by environment interactions: experience from Langhill. BSAP Occasional Publication 19, 5977.
Veerkamp, RF, Beerda, B, van der Lende, T 2003. Effects of genetic selection for milk yield on energy balance, levels of hormones, and metabolites in lactating cattle, and possible links to reduced fertility. Livestock Production Science 83, 257275.
Veerkamp, RF, Emmans, GC, Oldham, JD, Simm, G 1993. Energy and protein utilization of cows of high and low genetic merit for milk solids production on a high and low input diet. Biological basis of sustainable animal production. Proceedings of the 4th Zodiac Symposium, Wageningen, The Netherlands, April.
Veerkamp, RF, Oldenbroek, JK, van der Gaast, HJ, van der Werf, JHJ 2000. Genetic correlation between days until start of luteal activity and milk yield, energy balance and live weights. Journal of Dairy Science 83, 577583.
Verbyla, KL, Calus, MPL, Mulder, HA, de Haas, Y, Veerkamp, RF 2010. Predicting energy balance for dairy cows using high density SNP information. Journal of Dairy Science 93, 27572764.
Wall, E, Simm, G, Moran, D 2010. Developing breeding schemes to assist mitigation of greenhouse gas emissions. Animal 4, 366376.
Waters, SM, McCabe, MS, Howard, DJ, Giblin, L, Magee, DA, MacHugh, DE, Berry, DP 2011. Associations between newly discovered polymorphisms in the Bos taurus growth hormone receptor gene and performance traits in Holstein–Friesian dairy cattle. Animal Genetics 42, 3949.
Wolfe, BE, Metzger, ED, Stollar, C 1997. The effects of dieting on plasma tryptophan concentration and food intake in healthy women. Physiology & Behavior 61, 537541.



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