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Allele substitution and dominance effects of CD166/ALCAM gene polymorphisms for endoparasite resistance and test-day traits in a small cattle population using logistic regression analyses

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Abstract

The study investigated the effects of four single-nucleotide polymorphisms (SNPs) in the activated leukocyte cell adhesion molecule (ALCAM) gene on liver fluke (Fasciola hepatica) infections (FH-INF), gastrointestinal nematode infections (GIN-INF) and disease indicator traits [e.g. somatic cell score (SCS), fat-to-protein ratio (FPR)] in German dual-purpose cattle (DSN). A genome-wide association study inferred the chip SNP ALCAMc.73+32791A>G as a candidate for F. hepatica resistance in DSN. Because of the crucial function of ALCAM in immune responses, SNPs in the gene might influence further resistance and performance traits. Causal mutations were identified in exon 9 (ALCAMc.1017T>C) and intron 9 (ALCAMc.1104+10T>A, ALCAMc.1104+85T>C) in a selective subset of 94 DSN cows. We applied logistic regression analyses for the association between SNP genotypes with residuals for endoparasite traits (rINF-FH, rGIN-INF) and estimated breeding values (EBVs) for test-day traits. The probability of the heterozygous genotype was estimated in dependency of the target trait. Allele substitution effects for rFH-INF were significant for all four loci. The T allele of the SNPs ALCAMc.1017T>C and ALCAMc.1104+85T>C was the favourable allele when improving resistance against FH-INF. Significant allele substitution for rGIN-INF was only found for the chip SNP ALCAMc.73+32791A>G. We identified significant associations between the SNPs with EBVs for milk fat%, protein% and FPR. Dominance effects for the EBVs of test-day traits ranged from 0.00 to 0.47 SD and were in the direction of improved resistance for rFH-INF. We estimated favourable dominance effects from same genotypes for rFH-INF and FPR, but dominance effects were antagonistic between rFH-INF and SCS.

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References

  • Agneessens J, Clearebout E, Dorny P, Borgsteede FHM, Vercruysse J (2000) Nematode parasitism in adult dairy cows in Belgium. Vet Parasitol 90:83–92

    PubMed  CAS  Google Scholar 

  • Alam MBB, Omar AI, Faruque MO, Notter DR, Periasamy K, Mondal MMH et al (2019) Single nucleotide genes are significantly associated with resistance to Haemonchus contortus infection in goats. J Anim Sci Biotechnol 10:30

    PubMed  PubMed Central  Google Scholar 

  • Ali AKA, Shook GE (1980) An optimum transformation for somatic cell concentration in milk. J Dairy Sci 63:487–490

    Google Scholar 

  • Aliloo H, Pryce JE, González-Recio O, Cocks BG, Hayes BJ (2016) Accounting for dominance to improve genomic evaluations of dairy cows for fertility and milk production traits. Genet Sel Evol 48:8

    PubMed  PubMed Central  Google Scholar 

  • Alvarez Rojas CA, Ansell BRE, Hall RS, Gasser RB, Young ND, Jex AR, Scheerlinck J-PY (2015) Transcriptional analysis identifies key genes involved in metabolism, fibrosis/tissue repair and the immune response against Fasciola hepatica in sheep liver. Parasite Vector 8:124

    Google Scholar 

  • Bagheri M, Miraie-Ashtiani R, Moradi-Shahrbabak M, Nejati-Javaremi A, Pakdel A, von Borstel UU, Pimentel ECG, König S (2013) Selective genotyping and logistic regression analyses to identify favorable SNP-genotypes for clinical mastitis and production traits in Holstein dairy cattle. Livest Sci 151:140–151

    Google Scholar 

  • Beesley NJ, Williams DJL, Paterson S, Hodgkinson J (2017) Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance. Int J Parasitol 47:11–20

    PubMed  PubMed Central  CAS  Google Scholar 

  • Benavides MV, Weimer TA, Borba MFS, Berne MEA, Sacco AMS (2009) Genetic analyses of polymorphisms on ovine chromosomes 5 and 20 and their effect on resistance to internal parasites. Small Rumin Res 83:67–73

    Google Scholar 

  • Blanco-Penedo I, Höglund J, Fall N, Emanuelson U (2012) Exposure to pasture borne nematodes affects individual milk yield in Swedish dairy herds. Vet Parasitol 188:93–98

    PubMed  CAS  Google Scholar 

  • Bolormaa S, Pryce JE, Zhang Y, Reverter A, Barendse W, Hayes BJ, Goddard ME (2015) Non-additive genetic variation in growth, carcass and fertility traits of beef cattle. Genet Sel Evol 47:26

    PubMed  PubMed Central  Google Scholar 

  • Borgsteede FHM, Tibben J, Cornelissen JBWJ, Agneessens J, Gaasenbeek CPH (2000) Nematode parasites of adult dairy cattle in the Netherlands. Vet Parasitol 89:287–296

    PubMed  CAS  Google Scholar 

  • Bovenhuis H, Visker MHPW, van Valenberg HJF, Buitenhuis AJ, Arendok JAM (2015) Effects of the DGAT1 polymorphism on test-day milk production traits throughout lactation. J Dairy Sci 98:6572–6582

    PubMed  CAS  Google Scholar 

  • Brady MT (1999) Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infect Immun 67:5372–5378

    PubMed  PubMed Central  CAS  Google Scholar 

  • Calus MPL, Berry DP, Banos G, de Haas Y, Veerkamp RF (2013) Genomic selection: the option for new robustness traits? Adv Anim Biosci 4:618–625

    Google Scholar 

  • Caminade C, van Dijk J, Baylis M, Williams D (2015) Modelling recent and future climatic suitability for fasciolosis in Europe. Geosp Health 9:301–308

    Google Scholar 

  • Charlier J, van der Voort M, Kenyon F, Skuce P, Vercruysse J (2014) Chasing helminths and their economic impact on farmed ruminants. Trends Parasitol 30:361–367

    PubMed  Google Scholar 

  • Charon KM, Moskwa B, Rutkowski R, Gruszczyńska J, Świderek W (2002) Microsatellite polymorphism in DBR1 gene (MHC class II) and its relation to nematode faecal egg count in Polish Heath Sheep. J Anim Feed Sci 11:47–58

    Google Scholar 

  • Coppieters W, Mes THM, Druet T, Farnir F, Tamma N, Schrooten C, Cornelissen AWCA, Georges M, Ploeger HW (2009) Mapping QTL influencing gastrointestinal nematode burden in Dutch Holstein-Friesian dairy cattle. BMC Genomics 10:96

    PubMed  PubMed Central  Google Scholar 

  • Czarnik U, Galiński M, Pareek CS, Zabolewicz T, Wielgosz-Groth Z (2007) Study of an association between SNP 775C>T within the bvine ITBG2 gene and milk performance traits in Black and White cows. Czech J Anim Sci 52:1–6

    CAS  Google Scholar 

  • Dusza M, Pokorska J, Mukulska J, Kulaj D, Cupial M (2018) L-Selectin gene polymorphism and its association with clinical mastitis, somatic cell score, and milk production in Polish Holstein-Friesian cattle. Czech J Anim Sci 63:256–262

    CAS  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longmans Green, Harlow

    Google Scholar 

  • Foster N, Elsheikka HM (2012) The immune response to parasitic helminths of veterinary importance and its potential manipulation for future vaccine control strategies. Parasitol Res 110:1587–1599

    PubMed  Google Scholar 

  • Gengler N (1996) Persistency of lactation yields: a review. Interbull Bull 12:87–96

    Google Scholar 

  • Georges M, Charlier C, Hayes B (2019) Harnessing genomic information for livestock improvement. Nat Rev Genet 20:135–156

    PubMed  CAS  Google Scholar 

  • Gray GD (1997) The use of genetically resistant sheep to control nematode parasitism. Vet Parasitol 72:345–357

    PubMed  CAS  Google Scholar 

  • Han YP (2006) Matrix metalloproteinases, the pros and cons, in liver fibrosis. J Gastroenterol Hepatol 21(Suppl. 3):88–91

    Google Scholar 

  • Hanotte O, Ronin Y, Agaba M, Nilsson P, Gelhaus A, Horstmann R, Sugimoto Y, Kemp S, Gibson J, Korol A, Soller M, Teale A (2003) Mapping of quantitative trait loci controlling trypanotolerance in a cross of tolerant West African N’Dama and susceptible East African Boran cattle. Proc Natl Acad Sci USA 100:7443–7448

    PubMed  CAS  Google Scholar 

  • He Y, Chu Q, Ma P, Wang Y, Zhang Q, Sun D, Zhang Y, Yu Y, Zhang Y (2011) Association of bovine CD4 and STAT5b single nucleotide polymorphisms with somatic cell scores and milk production traits in Chinese Holsteins. J Dairy Res 78:242–249

    PubMed  CAS  Google Scholar 

  • Henshall JM, Goddard ME (1999) Multiple-trait mapping of quantitative trait loci after selective genotyping using logistic regression. Genetics 151:885–894

    PubMed  PubMed Central  CAS  Google Scholar 

  • Heriazon A, Quinton M, Miglior F, Leslie KE, Sears W, Mallard BA (2013) Phenotypic and genetic parameters of antibody and dalyed-type hypersensitivity responses of lactating Holstein cows. Vet Immunol Immunopathol 154:83–92

    PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    PubMed  CAS  Google Scholar 

  • Hill WG, Goddard ME, Visscher PM (2008) Data and theory point to mainly additive genetic variance for complex traits. PLoS Genet 4(2):e1000008

    PubMed  PubMed Central  Google Scholar 

  • Hillyer GV, Soler de Galanes M, Buchón P, Bjorland J (1996) Herd evaluation by enzyme-linked immunosorbent assay for the determination of Fasciola hepatica infection in sheep and cattle from Altiplano of Bolivia. Vet Parasitol 61:211–220

    PubMed  CAS  Google Scholar 

  • Huth F (1995) Laktation des Rindes. Verlag Eugen Ulmer, Stuttgart, Germany

    Google Scholar 

  • Ingale SL, Singh P, Raina OK, Verma AK, Channappanavar R, Mehra UR (2010) Interleukin-2 and interleukin-10 gene expression in calves experimentally infected with Fasciola gigantica. Livest Sci 131:141–143

    Google Scholar 

  • Kimura K, Goff JP, Kehrli ME (1999) Effects of the presence of the mammary gland on expression of neutrophil adhesion molecules and myeloperoxidase activity in periparturient dairy cows. J Dairy Sci 82:2385–2392

    PubMed  CAS  Google Scholar 

  • King JA, Ofori-Acquah SF, Stevens T, Al-Mehdi A-B, Fodstad O, Jiang WG (2004) Activated leukocyte cell adhesion molecule in breast cancer: prognostic indicator. Breast Cancer Res 6:478–487

    Google Scholar 

  • Klein S-L, Scheper C, Brügemann K, Swalve HH, König S (2019) Phenotypic relationships, genetic parameters, genome-wide associations, and identification of potential candidate genes for ketosis and fat-to-protein ratio in German Holstein cows. J Dairy Sci 102:6276–6287

    PubMed  CAS  Google Scholar 

  • Koeck A, Jamrozik J, Schenkel FS, Moore RK, Lefebvre DM, Kelton DF, Miglior F (2014) Genetic analysis of milk ß-hydroxybutyrate and its association with fat-to-protein ratio, body condition score, clinical ketosis, and displaced abomasums in early first lactation of Canadian Holsteins. J Dairy Sci 97:7286–7292

    PubMed  CAS  Google Scholar 

  • König S, Chang YM, von Borstel UU, Gianola D, Simianer H (2008) Genetic and phenotypic relationships among milk urea nitrogen, fertility, and milk yield in Holstein cows. J Dairy Sci 91:4372–4382

    PubMed  Google Scholar 

  • Konno A, Ahn JS, Kitamura H, Hamilton MJ, Gebe JA, Aruffo A, Davis WC (2001) Tissue distribution of CD6 and CD6 ligand in cattle: expression of the CD6 ligand (CD166) in the autonomic nervous system of cattle and the human. J Leukoc Biol 69:944–950

    PubMed  CAS  Google Scholar 

  • Kordalis NG, Arsenopoulos K, Vasileiou NGC, Mavrogianni VS, Lianou DT, Papadopoulos E, Fthenakis GC (2019) Field evidence for association between increased gastrointestinal nematode burden and subclinical mastitis in dairy sheep. Vet Parasitol 265:56–62

    PubMed  CAS  Google Scholar 

  • Korkuć P, Arends D, Scheper C, May K, König S, Brockmann GA (2017) 1-Step versus 2-step imputation: a case study in German Black Pied cattle. Proc World Congr Genet Appl Livest Prod 11:282

    Google Scholar 

  • Kozat S, Denizhan V (2010) Glucose, lipid, and lipoprotein levels in sheep naturally infected with Fasciola hepatica. J Parasitol 96:657–659

    PubMed  Google Scholar 

  • Kuehn C, Edel C, Weikard R, Thaller G (2007) Dominance and parent-of-origin effect of coding and non-coding alleles at the acylCoA-diacylglycerol-acyltransferase (DGAT1) gene on milk production traits in German Holstein cows. BMC Genet 8:62

    PubMed  PubMed Central  Google Scholar 

  • Kuerpick B, Schnieder T, Strube C (2012) Seasonal pattern of Fasciola hepatica antibodies in dairy herds in Northern Germany. Parasitol Res 111:1085–1092

    PubMed  Google Scholar 

  • Lei Z, Yuan-Yuan Y, Zhong-Hao L, Li-Juan K, Guan-Dong X, He-Shuang D, Gen-Liu W (2006) Detection and characterization of PCR-SSCP markers of the bovine lactoferrin gene for clinical mastitis. Asian-Aust J Anim Sci 19:1399–1403

    Google Scholar 

  • Lucena AN, Cuartero LG, Mulcahy G, Zintl A (2017) The immunomodulatory effects of co-infection with Fasciola hepatica: from bovine tuberculosis to Johne’s disease. Vet J 222:9–16

    Google Scholar 

  • Lunter PC, van Kilsdonk JWJ, van Beek H, Cornelissen IMHA, Bergers M, Willems PHGM, van Muijen GNP, Swart GWM (2005) Activated leukocyte cell adhesion molecule (ALCAM/CD166/MEMD), a novel actor in invasive growth, controls matrix metalloproteinase activity. Cancer Res 65:19

    Google Scholar 

  • Madsen P, Jensen J (2013) A user’s guide to DMU. A package for analysing multivariate mixed models. Version 6, release 5.2. Center for quantitative genetics and genomics. Dept. Of Molecular Biology and Genetics, University of Aarhus, Reserach Centre Foulum. Tjele, Denmark

  • Marshall K, Mugambi JM, Nagda S, Sonstegard TS, Van Tassell CP, Baker RL, Gibson JP (2013) Quantitative trait loci for resistance to Haemonchus contortus artificial challange in Red Maasai and Dorper sheep of East Africa. Anim Genet 44:285–295

    PubMed  CAS  Google Scholar 

  • May K, Brügemann K, König S, Strube C (2017) Patent gastrointestinal nematode infections in organically and conventionally pastured dairy cows and their impact on individual milk and fertility parameters. Vet Parasitol 245:119–127

    PubMed  Google Scholar 

  • May K, Scheper C, Brügemann K, Yin T, Strube C, Korkuć P, Brockmann GA, König S (2019) Genome-wide associations and functional gene analyses for endoparasite resistance in an endangered population of native German Black Pied cattle. BMC Genomics 20:227

    Google Scholar 

  • McClure J, Cromie AR, Sayers R, Graham D, Byrne N, Berry DP (2014) Genetics of susceptibility to bovine diarrhea virus, bovine herpesvirus type 1 and Fasciola hepatica in cattle. In: Proceedings of the 10th world congress of genetics applied to livestock production

  • Mendes EA, de Oliveira Mendes TA, dos Santos SL, Menezes-Souza D, Bartholomeu DC, Martins IV, Silva LM, Lima Wdos S (2013) Expression of IL-4, IL-10 and IFN-γ in the liver tissue of cattle that are naturally infected with Fasciola hepatica. Vet Parasitol 195:177–182

    PubMed  CAS  Google Scholar 

  • Mezo M, Gonzalez-Warleta M, Antonio Castro-Hermida J, Muino L, Ubeira FM (2011) Association between anti-F. hepatica antibody levels in milk and production losses in dairy cows. Vet Parasitol 180:237–242

    PubMed  Google Scholar 

  • Oviedo-Boyso J, Valdez-Alarcón Cajero-Juárez M, Ochoa-Zarzosa A, López-Meza JE, Bravo-Patiño Baizabal-Aguirre VM (2007) Innate immune response of bovine mammary gland pathogenic bacteria responsible for mastitis. J Infect 54:399–409

    PubMed  Google Scholar 

  • Pasandideh M, Mohammadabadi MR, Esmailizadeh AK, Tarang A (2015) Association of bovine PPARGC1A and OPN genes with milk production and composition in Holstein cattle. Czech J Anim Sci 60:97–104

    CAS  Google Scholar 

  • Perkins KH, VandeHaar MJ, Tempelman RJ, Burton JL (2001) Negative energy balance does not decrease expression of leukocyte adhesion or antigen-presenting molecules in cattle. J Dairy Sci 84:421–428

    PubMed  CAS  Google Scholar 

  • Phiri IK, Phiri AM, Harrison LJS (2007) The serum glucose and ß-hydroxybutyrate levels in sheep with experimental Fasciola hepatica and Fasciola gigantica infection. Vet Parasitol 143:287–293

    PubMed  CAS  Google Scholar 

  • Piedrafita D, Raadsma HW, Prowse R, Spithill TW (2004) Immunology of the host-parasite relationship in fasciolosis (Fasciola hepatica and Fasciola gigantica). Can J Zool 82:233–250

    Google Scholar 

  • Pryce JE, Haile-Mariam M, Verbyla K, Bowman PJ, Goddard ME, Hayes BJ (2010) Genetic markers for lactation persistency in primiparous Australian dairy cows. J Dairy Sci 93:2202–2214

    PubMed  CAS  Google Scholar 

  • R Core Team (2013) R: A language and environmental for statistical computing. R Core Team, Vienna

    Google Scholar 

  • Rajala-Schultz PJ, Saville WJA, Frazer GS, Wittum TE (2001) Asscoiation between milk urea nitrogen and feritlity in Ohio Dairy cows. J Dairy Sci 84:482–489

    PubMed  CAS  Google Scholar 

  • Ren G, Roberts AI, Shi Y (2011) Adhesion molecules. Cell Adhes Migr 5:1

    Google Scholar 

  • Roy B, Brahma B, Ghosh S, Pankaj PK, Mandal G (2011) Evaluation of milk urea concentration as useful indicator for dairy herd management: a review. Asian J Anim Vet Adv 6:1–19

    Google Scholar 

  • Ruiz-Campillo MT, Molina Hernandez V, Escamilla A, Stevenson M, Perez J, Martinez-Moreno A, Donnelly S, Dalton JP, Cwiklinski K (2017) Immune signatures of pathogenesis in the peritoneal compartment during early infection of sheep with Fasciola hepatica. Sci Rep 7:2782

    PubMed  PubMed Central  Google Scholar 

  • SAS Institute Inc (2013) Version 9.4. SAS Institute, Inc., Cary

  • Schwaiger F-W, Gostomski D, Stear MJ, Duncan JL, McKellar QA, Epplen JT, Buitkamp J (1995) An ovine Major Histocompatibility Complex DRB1 allele is associated with low faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Int J Parasitol 25:815–822

    PubMed  CAS  Google Scholar 

  • Schweizer G (2005) Estimating the financial losses due to bovine fasciolosis in Switzerland. Vet Rec 157:188–193

    PubMed  CAS  Google Scholar 

  • Sun C, VanRaden PM, Cole JB, O’Connell JR (2014) Improvement of prediction ability for genomic selection of dairy cattle by including dominance effects. PLoS ONE 9:e103934

    PubMed  PubMed Central  Google Scholar 

  • Swart GWM (2002) Activated leukocyte cell adhesion molecule (CD166/ALCAM): developmental and mechanistic aspects of cell clustering and cell migration. Eur J Cell Biol 81:313–321

    PubMed  CAS  Google Scholar 

  • Szyda J, Komisarek J, Antkowiak I (2014) Modelling effects of candidate genes on complex traits as variables over time. Anim Genet 45:322–328

    PubMed  CAS  Google Scholar 

  • Tao W, Mallard B, Karrow N, Bridle B (2003) Construction and application of a bovine immune-endocrine cDNA microarray. Vet Immunol Immunopathol 101:1–17

    Google Scholar 

  • Thienpont D, Rochette F, Vanparijs OFJ (1979) Diagnosing helminthiasis by coprological examination. Janssen Research Foundation, Beerse, Belgium, p 187

    Google Scholar 

  • Thompson-Crispi KA, Sewalem A, Miglior F, Mallard BA (2012) Genetic parameters of adaptive immune response traits in Candian Holsteins. J Dairy Sci 95:401–409

    PubMed  CAS  Google Scholar 

  • Tilquin P (2003) Methodological aspects of the mapping of disease resistance in livestock. Louvain-la-Neuve: Université catholique de Louvain, PhD thesis

  • Twomey AJ, Carroll RI, Doherty ML, Byrne N, Graham DA, Sayers RG, Blom A, Berry DP (2018) Genetic correlations between endo-parasite phenotypes and economically important traits in dairy and beef cattle. J Anim Sci 96:407–421

    PubMed  PubMed Central  Google Scholar 

  • Twomey AL, Berry DP, Evans RD, Doherty ML, Graham DA, Purfield DC (2019) Genome-wide association study of endo-parasite phenotypes using imputed whole-genome sequence data in dairy and beef cattle. Gen Sel Evol 51:15

    Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:71–74

    Google Scholar 

  • Vercruysse J, Charlier J, van Dijk J, Morgan ER, Geary T, von Samson-Himmelstjerna G, Claerebout E (2017) Control of helminth infections by 2030. Parasitology 145:1–10

    Google Scholar 

  • Wagner M, Bilinska M, Pokryszko-Dragan A, Sobczynski M, Cyrul M, Kusnierczyk P, Jasek M (2014) ALCAM and CD6—multiple sclerosis risk factors. J Neuroimmunol 276:98–103

    PubMed  CAS  Google Scholar 

  • Walker SM, Johnston C, Hoey EM, Fairweather I (2011) Population dynamics of the liver fluke, Fasciola hepatica: the effect of time and spatial separation on the genetic diversity of fluke populations in the Netherlands. Parasitology 138:215–223

    PubMed  CAS  Google Scholar 

  • Weidle UH, Eggle D, Klostermann S, Swart GWM (2010) ALCAM/CD166: cancer-related Issues. Cancer Genomics Proteomics 7:231–244

    PubMed  CAS  Google Scholar 

  • Wolfinger R, O’Connel M (1993) Generalized linear mixed models: a pseudo-likelihood approach. J Stat Comput Simul 48:233–243

    Google Scholar 

  • Zhang FK, Hou JL, Guo AJ, Tian AL, Sheng ZA, Zheng WB, Huang WY, Elsheikka HM, Zhu XQ (2018) Expression profiles of genes involved in TLRs and NLRs signaling pathways of water buffaloes infected with Fasciola gigantica. Mol Immunol 94:18–26

    PubMed  CAS  Google Scholar 

  • Zheng M, Zhang L, Yu Hongsong HuJ, Cao Q, Huang G, Huang Y, Yuan G, Kijlstra A, Yan P (2016) Genetic polymorphisms of cell adhesion molecules in Behcet’s disease in a Chinese Han population. Sci Rep 6:24974

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou P, Du L-F, Lv G-Q, Yu X-M, Gu Y-L, Li J-P, Zhang C (2011) Functional polymorphisms in CD166/ALCAM gene associated with increased risk for breast cancer in a Chinese population. Breast Cancer Res Treat 128:527–534

    PubMed  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the German Federal Ministry of Food and Agriculture (BMEL) based on a decision of the Parliament of the Federal Republic of Germany, granted by the Federal Office for Agriculture and Food (BLE; grant number FKZ 2818BM090 and -091). We gratefully thank the H. Wilhelm Schaumann foundation for the provision of a PhD grant to KM.

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May, K., Weimann, C., Scheper, C. et al. Allele substitution and dominance effects of CD166/ALCAM gene polymorphisms for endoparasite resistance and test-day traits in a small cattle population using logistic regression analyses. Mamm Genome 30, 301–317 (2019). https://doi.org/10.1007/s00335-019-09818-z

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