A genome-wide association study of social genetic effects in Landrace pigs

  • Hong, Joon Ki ;
  • Jeong, Yong Dae ;
  • Cho, Eun Seok ;
  • Choi, Tae Jeong ;
  • Kim, Yong Min ;
  • Cho, Kyu Ho ;
  • Lee, Jae Bong ;
  • Lim, Hyun Tae ;
  • Lee, Deuk Hwan
  • Received : 2017.06.08
  • Accepted : 2017.11.05
  • Published : 2018.06.01


Objective: The genetic effects of an individual on the phenotypes of its social partners, such as its pen mates, are known as social genetic effects. This study aims to identify the candidate genes for social (pen-mates') average daily gain (ADG) in pigs by using the genome-wide association approach. Methods: Social ADG (sADG) was the average ADG of unrelated pen-mates (strangers). We used the phenotype data (16,802 records) after correcting for batch (week), sex, pen, number of strangers (1 to 7 pigs) in the pen, full-sib rate (0% to 80%) within pen, and age at the end of the test. A total of 1,041 pigs from Landrace breeds were genotyped using the Illumina PorcineSNP60 v2 BeadChip panel, which comprised 61,565 single nucleotide polymorphism (SNP) markers. After quality control, 909 individuals and 39,837 markers remained for sADG in genome-wide association study. Results: We detected five new SNPs, all on chromosome 6, which have not been associated with social ADG or other growth traits to date. One SNP was inside the prostaglandin $F2{\alpha}$ receptor (PTGFR) gene, another SNP was located 22 kb upstream of gene interferon-induced protein 44 (IFI44), and the last three SNPs were between 161 kb and 191 kb upstream of the EGF latrophilin and seven transmembrane domain-containing protein 1 (ELTD1) gene. PTGFR, IFI44, and ELTD1 were never associated with social interaction and social genetic effects in any of the previous studies. Conclusion: The identification of several genomic regions, and candidate genes associated with social genetic effects reported here, could contribute to a better understanding of the genetic basis of interaction traits for ADG. In conclusion, we suggest that the PTGFR, IFI44, and ELTD1 may be used as a molecular marker for sADG, although their functional effect was not defined yet. Thus, it will be of interest to execute association studies in those genes.


Candidate Genes;Social Genetic Effect;Average Daily Gain;Porcine Genome


  1. Bijma P, Wade MJ. The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection. J Evol Biol 2008;21:1175-88.
  2. McGlothlin JW, Moore AJ, Wolf JB, Brodie III ED. Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 2010;64:2558-74.
  3. Bergsma R, Kanis E, Knol EF, Bijma P. The contribution of social effects to heritable variation in finishing traits of domestic pigs (Sus scrofa). Genetics 2008;178:1559-70.
  4. Ellen E, Visscher J, Van Arendonk J, Bijma P. Survival of laying hens: genetic parameters for direct and associative effects in three purebred layer lines. Poult Sci 2008;87:233-9.
  5. Alemu SW, Bijma P, Moller SH, Janss L, Berg P. Indirect genetic effects contribute substantially to heritable variation in aggression- related traits in group-housed mink (Neovison vison). Genet Sel Evol 2014;46:30.
  6. Camerlink I, Turner SP, Bijma P, Bolhuis JE. Indirect genetic effects and housing conditions in relation to aggressive behaviour in pigs. PloS one 2013;8:e65136.
  7. Reimert I, Rodenburg TB, Ursinus WW, Kemp B, Bolhuis JE. Responses to novel situations of female and castrated male pigs with divergent social breeding values and different backtest classifications in barren and straw-enriched housing. Appl Anim Behav Sci 2014;151:24-35.
  8. Reimert I, Rodenburg TB, Ursinus WW, et al. Backtest and novelty behavior of female and castrated male piglets, with diverging social breeding values for growth. J Anim Sci 2013; 91:4589-97.
  9. Hu Z-L, Park CA, Wu X-L, Reecy JM. Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic Acids Research 2013;41:D871-D9.
  10. Yang J, Zaitlen NA, Goddard ME, Visscher PM, Price AL. Advantages and pitfalls in the application of mixed-model association methods. Nat Genet 2014;46:100-6.
  11. Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 2000;80:1-29.
  12. Gadsby JE, Lovdal JA, Britt JH, Fitz TA. Prostaglandin F2 alpha receptor concentrations in corpora lutea of cycling, pregnant, and pseudopregnant pigs. Biol Reprod 1993;49:604-8.
  13. Estill CT, Britt JH, Gadsby JE. Repeated administration of prostaglandin F2 alpha during the early luteal phase causes premature luteolysis in the pig. Biol Reprod 1993;49:181-5.
  14. Hemsworth PH, Tilbrook AJ. Sexual behavior of male pigs. Horm Behav 2007;52:39-44.
  15. Camerlink I, Ursinus WW, Bijma P, Kemp B, Bolhuis JE. Indirect genetic effects for growth rate in domestic pigs alter aggressive and manipulative biting behaviour. Behav Genet 2015;45: 117-26.
  16. Kitamura A, Takahashi K, Okajima A, Kitamura N. Induction of the human gene for p44, a hepatitis‐C‐associated microtubular aggregate protein, by interferon‐alpha/beta. Eur J Biochem 1994;224:877-83.
  17. Liu C, Zhu H, Subramanian GM, Moore PA, Xu Y, Nelson DR. Anti‐hepatitis C virus activity of albinterferon alfa‐2b in cell culture. Hepatol Res 2007;37:941-7.
  18. Hallen LC, Burki Y, Ebeling M, et al. Antiproliferative activity of the human IFN-${\alpha}$-inducible protein IFI44. J Interferon Cytokine Res 2007;27:675-80.
  19. Green TJ, Dixon TJ, Devic E, Adlard RD, Barnes AC. Differential expression of genes encoding anti-oxidant enzymes in Sydney rock oysters, Saccostrea glomerata (Gould) selected for disease resistance. Fish Shellfish Immunol 2009;26:799-810.
  20. Power D, Santoso N, Dieringer M, et al. IFI44 suppresses HIV-1 LTR promoter activity and facilitates its latency. Virology 2015; 481:142-50.
  21. Koistinaho M, Koistinaho J. Role of p38 and p44/42 mitogenactivated protein kinases in microglia. Glia 2002;40:175-83.
  22. Ueyama T, Senba E, Kasamatsu K, et al. Molecular mechanism of emotional stress‐induced and catecholamine‐induced heart attack. J Cardiovasc Pharmacol 2003;41:S115-S8.
  23. Asher L, Friel M, Griffin K, Collins LM. Mood and personality interact to determine cognitive biases in pigs. Biol Lett 2016; 12:20160402.
  24. Nechiporuk T, Urness LD, Keating MT. ETL, a Novel Seventransmembrane Receptor That Is Developmentally Regulated in the Heart. ETL is a member of the secretin family and belons to the epidermal growth factor-seven-transmembane subfamily. J Biol Chem 2001;276:4150-7.
  25. Masiero M, Simoes FC, Han HD, et al. A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell 2013;24:229-41.
  26. Lee KT, Byun MJ, Kang KS, et al. Neuronal genes for subcutaneous fat thickness in human and pig are identified by local genomic sequencing and combined SNP association study. PLoS One 2011;6:e16356.
  27. Agrawal A, Lynskey MT, Bucholz KK, et al. DSM-5 cannabis use disorder: a phenotypic and genomic perspective. Drug Alcohol Depend 2014;134:362-9.
  28. Arango J, Misztal I, Tsuruta S, Culbertson M, Herring W. Estimation of variance components including competitive effects of Large White growing gilts. J Anim Sci 2005;83:1241-6.
  29. McGlone JJ, Morrow JL. Reduction of pig agonistic behavior by androstenone. J Anim Sci 1988;66:880-4.
  30. Duijvesteijn N, Knol EF, Merks JW, et al. A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6. BMC Genet 2010;11:42.


Supported by : Rural Development Administration in Republic of Korea