Article | Published:

Nature vs. nurture in human sociality: multi-level genomic analyses of social conformity

Journal of Human Geneticsvolume 63pages605619 (2018) | Download Citation

Abstract

Social conformity is fundamental to human societies and has been studied for more than six decades, but our understanding of its mechanisms remains limited. Individual differences in conformity have been attributed to social and cultural environmental influences, but not to genes. Here we demonstrate a genetic contribution to conformity after analyzing 1,140 twins and single-nucleotide polymorphism (SNP)-based studies of 2,130 young adults. A two-step genome-wide association study (GWAS) revealed replicable associations in 9 genomic loci, and a meta-analysis of three GWAS with a sample size of ~2,600 further confirmed one locus, corresponding to the NAV3 (Neuron Navigator 3) gene which encodes a protein important for axon outgrowth and guidance. Further multi-level (haplotype, gene, pathway) GWAS strongly associated genes including NAV3, PTPRD (protein tyrosine phosphatase receptor type D), ARL10 (ADP ribosylation factor-like GTPase 10), and CTNND2 (catenin delta 2), with conformity. Magnetic resonance imaging of 64 subjects shows correlation of activation or structural features of brain regions with the SNPs of these genes, supporting their functional significance. Our results suggest potential moderate genetic influence on conformity, implicate several specific genetic elements in conformity and will facilitate further research on cellular and molecular mechanisms underlying human conformity.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Sherif M. The Psychology of Social Norms. New York, NY, USA: Harper & Brothers; 1936.

  2. 2.

    Asch SE. in Effects of group pressure upon the modification and distortion of judgements. (ed.) Guetzkow H. Groups, leadership and men. Pittsburgh, PA, USA: Carnegie Press; 1951. p. 177–190.

  3. 3.

    Asch SE. Studies of independence and conformity: 1. A minority of one against a unanimous majority. Psychol Monogr. 1956;70:1–70.

  4. 4.

    Crutchfield RS. Conformity and character. Am Psychol. 1955;10:191–8.

  5. 5.

    Cialdini RB, Goldstein NJ. Social influence: compliance and conformity. Annu Rev Psychol. 2004;55:591–621.

  6. 6.

    Grofman B, Feld SL. Rousseaus general will—a condorcetian perspective. Am Polit Sci Rev. 1988;82:567–76.

  7. 7.

    Kendal J, Giraldeau L, Laland K. The evolution of social learning rules: payoff-biased and frequency-dependent biased transmission. J Theor Biol. 2009;260:210–9.

  8. 8.

    Bond R, Smith PB. Culture and conformity: a meta-analysis of studies using Asch’s (1952b, 1956) Line judgment task. Psychol Bull. 1996;119:111–37.

  9. 9.

    Raafat RM, Chater N, Frith C. Herding in humans. Trends Cogn Sci. 2009;13:420–8.

  10. 10.

    Stein R. The pull of the group: conscious conflict and the involuntary tendency towards conformity. Conscious Cogn. 2013;22:788–94.

  11. 11.

    Berns GS, Chappelow J, Zink CF, Pagnoni G, Martin-Skurski ME, Richards J. Neurobiological correlates of social conformity and independence during mental rotation. Biol Psychiatry. 2005;58:245–53.

  12. 12.

    Edelson MG, Sharot T, Dolan RJ, Dudai Y. Following the crowd: brain substrates of long-term memory conformity. Science. 2011;333:108–11.

  13. 13.

    Galef B, Whiskin E. ‘Conformity’ in Norway rats? Anim Behav. 2008;75:2035–9.

  14. 14.

    Claidiere N, Whiten A. Integrating the study of conformity and culture in humans and nonhuman animals. Psychol Bull. 2012;138:126–45.

  15. 15.

    Whiten A, Horner V, de Waal FB. Conformity to cultural norms of tool use in chimpanzees. Nature. 2005;437:737–40.

  16. 16.

    van de Waal E, Borgeaud C, Whiten A. Potent social learning and conformity shape a wild primate’s foraging decisions. Science. 2013;340:483–5.

  17. 17.

    Corriveau KH, Harris PL. Preschoolers (sometimes) defer to the majority in making simple perceptual judgments. Dev Psychol. 2010;46:437–45.

  18. 18.

    Powell LJ, Spelke ES. Preverbal infants expect members of social groups to act alike. Proc Natl Acad Sci USA. 2013;110:E3965–3972.

  19. 19.

    Kim H, Markus HR. Deviance or uniqueness, harmony or conformity? A cultural analysis. J Pers Soc Psychol. 1999;77:785–800.

  20. 20.

    Triandis HC. in Cross-cultural studies of individualism and collectivism. (ed.) Berman JJ. Nebraska symposium on motivation. Lincoln, NE, USA: University of Nebraska Press; 1989. p. 41–133.

  21. 21.

    Takano Y, Sogon S. Are Japanese more collectivistic than Americans? Examining conformity in in-groups and the reference-group effect. J Cross Cult Psychol. 2008;39:237–50.

  22. 22.

    Kasser T, Koestner R, Lekes N. Early family experiences and adult values: a 26-year, prospective longitudinal study. Pers Soc Psychol Bull. 2002;28:826–35.

  23. 23.

    Wright DB, London K, Waechter M. Social anxiety moderates memory conformity in adolescents. Appl Cogn Psychol. 2010;24:1034–45.

  24. 24.

    Galinsky AD, Magee JC, Gruenfeld DH, Whitson JA, Liljenquist KA. Power reduces the press of the situation: implications for creativity, conformity, and dissonance. J Pers Soc Psychol. 2008;95:1450–66.

  25. 25.

    de Young CG, Peterson JB, Higgins DM. Higher-order factors of the Big Five predict conformity: are there neuroses of health? Pers Indiv Differ. 2002;33:533–52.

  26. 26.

    Klucharev V, Hytonen K, Rijpkema M, Smidts A, Fernandez G. Reinforcement learning signal predicts social conformity. Neuron. 2009;61:140–51.

  27. 27.

    Campbell-Meiklejohn DK, Bach DR, Roepstorff A, Dolan RJ, Frith CD. How the opinion of others affects our valuation of objects. Curr Biol. 2010;20:1165–70.

  28. 28.

    Izuma K, Adolphs R. Social manipulation of preference in the human brain. Neuron. 2013;78:563–73.

  29. 29.

    Stallen M, Smidts A, Sanfey AG. Peer influence: neural mechanisms underlying in-group conformity. Front Hum Neurosci. 2013;7:1–7.

  30. 30.

    Klucharev V, Munneke MAM, Smidts A, Fernandez G. Down regulation of the posterior medial frontal cortex prevents social conformity. J Neurosci. 2011;31:11934–40.

  31. 31.

    Constantino JN, Todd RD. Genetic structure of reciprocal social behavior. Am J Psychiatry. 2000;157:2043–5.

  32. 32.

    Rushton JP, Fulker DW, Neale MC, Nias DKB, Eysenck HJ. Altuism and aggression: the heritability of individual differences. J Pers Soc Psychol. 1986;50:1192–8.

  33. 33.

    Li XT, Zhang JD, Huang Y, Xu M, Liu J. Nurtured to follow the crowd: a twin study on conformity. Chin Sci Bull. 2013;58:1175–80.

  34. 34.

    Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet. 2006;38:904–9.

  35. 35.

    Neale MC, Boker SM, Xie G, Maes HH. Mx: Statistical modeling. Richmond, VA, USA: Department of Psychiatry, Virginia Commonwealth University; 2003.

  36. 36.

    Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet. 2010;42:565–9.

  37. 37.

    Yang J, Lee SH, Goddard ME, Visscher PM. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011;88:76–82.

  38. 38.

    Visscher PM, Hemani G, Vinkhuyzen AA, Chen GB, Lee SH, Wray NR, et al. Statistical power to detect genetic (co)variance of complex traits using SNP data in unrelated samples. PLoS Genet. 2014;10:e1004269.

  39. 39.

    Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75.

  40. 40.

    Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21:263–5.

  41. 41.

    Gauderman WJ, Morrison JM. QUANTO 1.1: a computer program for power and sample size calculations for genetic-epidemiology studies. 2006. http://hydra.usc.edu/gxe.

  42. 42.

    Howie B, Fuchsberger C, Stephens M, Marchini J, Abecasis GR. Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nat Genet. 2012;44:955–9.

  43. 43.

    Howie BN, Donnelly P, Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009;5:e1000529.

  44. .44.

    Marchini J, Howie B, Myers S, McVean G, Donnelly P. A new multipoint method for genome-wide association studies via imputation of genotypes. Nat Genet. 2007;39:906–13.

  45. 45.

    Pruim RJ, Welch RP, Sanna S, Teslovich TM, Chines PS, Gliedt TP. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics. 2010;26:2336–7.

  46. 46.

    Liu JZ, Tozzi F, Waterworth DM, Pillai SG, Muglia P, Middleton L, et al. Meta-analysis and imputation refines the association of 15q25 with smoking quantity. Nat Genet. 2010;42:436–40.

  47. 47.

    Chanda P, Huang H, Arking DE, Bader JS. Fast association tests for genes with FAST. PLoS ONE. 2013;8:e68585.

  48. 48.

    Liu JZ, McRae AF, Nyholt DR, Medland SE, Wray NR, Brown KM, et al. A versatile gene-based test for genome-wide association studies. Am J Hum Genet. 2010;87:139–45.

  49. 49.

    de Leeuw CA, Mooij JM, Heskes T, Posthuma D. MAGMA: Generalized gene-set analysis of GWAS data. PLoS Comput Biol. 2015;11:e1004219.

  50. 50.

    Nam D, Kim J, Kim SY, Kim S. GSA-SNP: a general approach for gene set analysis of polymorphisms. Nucleic Acids Res. 2010;38:W749–W754.

  51. 51.

    Segrè AV, DIAGRAM Consortium, MAGIC investigators, Groop, L., Mootha VK, Daly MJ, et al. Common inherited variation in mitochondrial genes is not enriched for associations with Type 2 diabetes or related glycemic traits. PLoS Genet. 2010;6:e1001058.

  52. 52.

    Brett M, Jean-Luc A, Valabregue R, Jean-Baptiste P. Region of interest analysis using an SPM toolbox. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan. Available in CD-ROM in Neuroimage 2002;16 (abstract).

  53. 53.

    Reysen M. The effects of conformity on recognition judgements. Memory. 2005;13:87–94.

  54. 54.

    Horry R, Palmer MA, Sexton M, Brewer N. Memory conformity for confidently recognized items: the power of social influence on memory reports. J Exp Soc Psychol. 2012;48:783–6.

  55. 55.

    Agrawal A, Dick DM, Bucholz KK, Madden PAF, Cooper ML, Sher KJ, et al. Drinking expectancies and motives: a genetic study of young adult women. Addiction. 2008;103:194–204.

  56. 56.

    Kristjansson SD, Agrawal A, Littlefield AK, Pergadia ML, Lessov-Schlaggar CN, Sartor CE, et al. Drinking motives in female smokers: factor structure, alcohol dependence, and genetic influences. Alcohol Clin Exp Res. 2011;35:345–54.

  57. 57.

    Rushton JP. Genetic and environmental contributions to pro-social attitudes: a twin study of social responsibility. Proc Biol Sci. 2004;271:2583–5.

  58. 58.

    Jacobs N, Gestel SV, Derom C, Thiery E, Vernon P, Derom R, et al. Heritability estimates of intelligence in twins: effect of chorion type. Behav Genet. 2001;31:209–17.

  59. 59.

    Jang KL, Livesley WJ, Vernon PA. Heritability of the big five personality dimensions and their facets: a twin study. J Pers. 1996;64:577–91.

  60. 60.

    Maes T, Barcelo A, Buesa C. Neuron navigator: a human gene family with homology to unc-53, a cell guidance gene from Caenorhabditis elegans. Genomics. 2002;80:21–30.

  61. 61.

    Peeters PJ, Baker AK, Goris I, Daneels G, Verhasselt P, Luyten WH, et al. Sensory deficits in mice hypomorphic for a mammalian homologue of unc-53. Brain Res Dev Brain Res. 2004;150:89–101.

  62. 62.

    Kosik KS, Donahue CP, Israely I, Liu X, Ochiishi T. Delta-catenin at the synaptic-adherens junction. Trends Cell Biol. 2005;15:172–8.

  63. 63.

    Nivard MG, Mbarek H, Hottenga JJ, Smit JH, Jansen R, Penninx BW, et al. Further confirmation of the association between anxiety and CTNND2: replication in humans. Genes Brain Behav. 2014;13:195–201.

  64. 64.

    Vrijenhoek T, Buizer-Voskamp JE, van der Stelt I, Strengman E, Genetic Risk and Outcome in Psychosis (GROUP) Consortium, Sabatti CG, et al. Recurrent CNVs disrupt three candidate genes in schizophrenia patients. Am J Hum Genet. 2008;83:504–10.

  65. 65.

    Cervenka S, Gustavsson JP, Halldin C, Farde L. Association between striatal and extrastriatal dopamine D2-receptor binding and social desirability. Neuroimage. 2010;50:323–8.

  66. 66.

    Egerton A, Rees E, Bose SK, Lappin J, Stokes PR, Turkheimer FE, et al. Truth, lies or self-deception? Striatal D(2/3) receptor availability predicts individual differences in social conformity. Neuroimage. 2010;53:777–81.

  67. 67.

    Campbell-Meiklejohn DK, Simonsen A, Jensen M, Wohlert V, Gjerloff T, Scheel-Kruger J, et al. Modulation of social influence by methylphenidate. Neuropsychopharmacology. 2012;37:1517–25.

  68. 68.

    Stallen M, de Dreu CK, Shalvi S, Smidts A, Sanfey AG. The herding hormone oxytocin stimulates in-group conformity. Psychol Sci. 2012;23:1288–92.

  69. 69.

    Huang Y, Kendrick KM, Zheng H, Yu R. Oxytocin enhances implicit social conformity to both in-group and out-group opinions. Psychoneuroendocrinology. 2015;60:114–9.

  70. 70.

    Wei Z, Zhao Z, Zheng Y. Neural mechanisms underlying social conformity in an ultimatum game. Front Hum Neurosci. 2013;7:896.

  71. 71.

    Edelson MG, Dudai Y, Dolan RJ, Sharot T. Brain substrates of recovery from misleading influence. J Neurosci. 2014;34:7744–53.

  72. 72.

    Milham MP, Banich MT. Anterior cingulate cortex: an fMRI analysis of conflict specificity and functional differentiation. Hum Brain Mapp. 2005;25:328–35.

  73. 73.

    Rudie JD, Shehzad Z, Hernandez LM, Colich NL, Bookheimer SY, Iacoboni M, et al. Reduced functional integration and segregation of distributed neural systems underlying social and emotional information processing in autism spectrum disorders. Cereb Cortex. 2012;22:1025–37.

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Project 31421003); the Beijing Advanced Innovation Center for Genomics at Peking University; the Peking-Tsinghua Center for Life Sciences; the Applied Development Program from the Science and Technology Committee of Chongqing (Grant number cstc2014yykfB10003, cstc2015shms-ztzx10006); and the Program of Mass Creativities Workshops from the Science and Technology Committee of Chongqing. We are grateful to Dr. Chen Wu, Dr. Jurg Ott, and Dr. Houfeng Zheng for comments on the manuscript, and to Zhangyan Guan and Huizhen Yang for help with DNA preparation.

Author information

Affiliations

  1. Peking-Tsinghua Center for Life Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Advanced Innovation Center for Genomics, Peking University, 100871, Beijing, China

    • Biqing Chen
    • , Zijian Zhu
    • , Yingying Wang
    • , Wan Fang
    •  & Yi Rao
  2. Affiliated Hospital of Nanjing University of Chinese Medicine, Jiangsu Province Hospital of Traditional Chinese Medicine, 210029, Nanjing, China

    • Biqing Chen
  3. State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-Sen University, 510060, Guangzhou, China

    • Xiaohu Ding
    •  & Mingguang He
  4. Department of Statistical Science, School of Mathematics, Sun Yat-Sen University, 510275, Guangzhou, China

    • Xiaobo Guo
  5. College of Laboratory Medicine, Chongqing Medical University, 400016, Chongqing, China

    • Qin Zhou
    • , Han Lei
    • , Ailong Huang
    •  & Tingmei Chen
  6. University-Town Hospital, Chongqing Medical University, 401331, Chongqing, China

    • Shanbi Zhou
  7. MOE Key Laboratory of Medical Diagnostics, Division of Molecular Nephrology and Creative Training Center for Undergraduates, College of Laboratory Medicine, Chongqing Medical University, 400016, Chongqing, China

    • Dongsheng Ni
    • , Yuping Gu
    •  & Jianing Liu

Authors

  1. Search for Biqing Chen in:

  2. Search for Zijian Zhu in:

  3. Search for Yingying Wang in:

  4. Search for Xiaohu Ding in:

  5. Search for Xiaobo Guo in:

  6. Search for Mingguang He in:

  7. Search for Wan Fang in:

  8. Search for Qin Zhou in:

  9. Search for Shanbi Zhou in:

  10. Search for Han Lei in:

  11. Search for Ailong Huang in:

  12. Search for Tingmei Chen in:

  13. Search for Dongsheng Ni in:

  14. Search for Yuping Gu in:

  15. Search for Jianing Liu in:

  16. Search for Yi Rao in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Yi Rao.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

DOI

https://doi.org/10.1038/s10038-018-0418-y

Article notes

These authors contributed equally: Biqing Chen and Zijian Zhu