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Aggression, Digit Ratio and Variation in Androgen Receptor and Monoamine Oxidase A Genes in Men

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Abstract

Variation in prenatal exposure to androgens is thought to be responsible for some of the individual differences in aggressive behavior among adults. A putative indicator of prenatal testosterone exposure, 2D:4D (the index to ring finger length) ratios have shown a weak correlation with aggression. Variation in sensitivity of the androgen receptor, resulting from polymorphism in the AR gene, is also thought to influence the relative expression of sexually dimorphic traits within each sex, including aggressive behavior and 2D:4D. Here we examine variation in aggression, 2D:4D, and polymorphism in the AR and MAO-A genes in a sample of 188 men. We find no evidence of AR gene influence on right hand 2D:4D, and a weak trend towards more feminine-typical left hand 2D:4D in men with more sensitive androgen receptors. Men with more sensitive androgen receptors tended to score lower on many of the subscales of the Aggression Questionnaire and Indirect Aggression Questionnaire. We found no influence of MAO-A allele on either digit ratio or aggressive behavior. We conclude that more masculine-typical 2D:4D does not reflect greater sensitivity to testosterone through variation in this locus on the AR gene, and that AR alleles conferring greater sensitivity to testosterone are associated with lower, not higher propensity to aggression.

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References

  • Abramovich DR, Rowe P (1973) Foetal plasma testosterone levels and midpregnancy and at term: relationship to foetal sex. J Endocrinol 56:621–622

    Article  PubMed  Google Scholar 

  • Abramovich DR, Davidson IA, Longstaff A, Pearson CK (1985) When does sexual differentiation of the human brain occur? In: Jones CT, Nathanielz PW (eds) The physiological development of the fetus and newborn. Academic, London, pp 659–662

    Google Scholar 

  • Archer J (1988) The behavioral biology of aggression. Cambridge University Press, New York

    Google Scholar 

  • Archer J (1991) The influence of testosterone on human aggression. Br J Psychol 82:1–28

    Article  PubMed  Google Scholar 

  • Archer J (2004) Sex differences in aggression in real-world settings: a meta-analytic review. Rev Gen Psychol 8:291–322

    Article  Google Scholar 

  • Baghaei F, Rosmond R, Landén M, Westberg L, Hellstrand M, Holm G, Eriksson E, Björntorp P (2003) Phenotypic and genotypic characteristics of women in relation to personality traits. Int J Behav Med 10:364–378

    Article  Google Scholar 

  • Bailey AA, Hurd PL (2005) Finger length ratio predicts physical aggression in men but not women. Biol Psychiatry 68:215–222

    Article  Google Scholar 

  • Benderlioglu Z, Nelson RJ (2004) Digit length ratios predict reactive aggression in women but not in men. Horm Behav 46:558–564

    Article  PubMed  Google Scholar 

  • Berenbaum SA, Bryk KK, Nowak N, Quigley CA, Moffat S (2009) Fingers as a marker of prenatal androgen exposure. Endocrinology 150:5119–5124

    Article  PubMed  Google Scholar 

  • Bjorkqvist K, Lagerspetz K, Kaukiainen A (1992) Do girls manipulate and do boys fight? Developmental trends in regard to direct and indirect aggression. Aggress Behav 18:117–127

    Article  Google Scholar 

  • Brown CJ, Goss SJ, Lubahn DB, Joseph DR, Wilson EM, French FS, Willard HF (1989) Androgen receptor locus on the human x-chromosome—regional localization to Xq11-12 and description of a DNA polymorphism. Am J Hum Genet 44:264–269

    PubMed  Google Scholar 

  • Buckholtz JW, Meyer-Lindenberg A (2008) MAOA and the neurogenetic architecture of human aggression. Trends Neurosci 31:120–129

    Article  PubMed  Google Scholar 

  • Buss AH, Perry M (1992) The aggression questionnaire. J Pers Soc Psychol 63:452–459

    Article  PubMed  Google Scholar 

  • Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2002) Role of genotype in the cycle of violence in maltreated children. Science 297:851–854

    Article  PubMed  Google Scholar 

  • Chamberlain NL, Driver ED, Miesfeld RL (1994) The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res 22:3181–3186

    Article  PubMed  Google Scholar 

  • Cheng D, Hong C-J, Liao D-L, Tsai S-J (2006) Association study of androgen receptor CAG repeat polymorphism and male violent criminal activity. Psychoneuroendocrinology 31:548–552

    Article  PubMed  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale, NJ

    Google Scholar 

  • Cohen-Bendahan CC, van de Beek C, Berenbaum SA (2005) Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav Rev 29:353–384

    Article  PubMed  Google Scholar 

  • Coyne SM, Manning JT, Ringer L, Bailey L (2007) Directional asymmetry (right–left differences) in digit ratio (2D:4D) predict indirect aggression in women. Pers Individ Diff 43:865–872

    Article  Google Scholar 

  • Crabbe P, Bogaert V, De Bacquer D, Goemaere S, Zmierczak H, Kaufman JM (2007) Part of the interindividual variation in serum testosterone levels in healthy men reflects differences in androgen sensitivity and feedback set point: contribution of the androgen receptor polyglutamine tract polymorphism. J Clin Endocrinol Metab 92:3604–3610

    Article  PubMed  Google Scholar 

  • Dogan A, Barut C, Konuk N, Bilge Y (2007) Relation of 2D : 4D ratio to aggression and anger. Neurol Psychiatr Brain Res 14:151–158

    Google Scholar 

  • Efron B, Tibshirani RJ (1994) An introduction to the bootstrap. Chapman & Hall, New York

    Google Scholar 

  • Finegan J-A, Bartelman B, Wong PY (1989) A window for the study of prenatal sex hormone influences on prenatal development. J Genet Psychol 150:101–112

    Article  PubMed  Google Scholar 

  • Forrest S, Eatough V, Shevlin M (2005) Measuring adult indirect aggression: the development and psychometric assessment of the indirect aggression scale. Aggress Behav 31:84–97

    Article  Google Scholar 

  • Forstmeier W, Rochester J, Millam JR (2008) Digit ratio unaffected by estradiol treatment of zebra finch nestlings. Gen Comp Endocrinol 156:379–384

    Article  PubMed  Google Scholar 

  • Forstmeier W, Muller JC, Kempenaers B (2010) A polymorphism in the oestrogen receptor gene explains covariance between digit ratio and mating behaviour. Proc R Soc B. doi:10.1098/rspb.2010.1007

  • Fraley RC, Marks MJ (2007) The null hypothesis significance-testing debate and its implications for personality research. In: Robins RW, Fraley RC, Kruger RF (eds) Handbook of research methods in personality psychology. Guilford Press, NY, pp 149–169

  • Gallup AC, White DD, Gallup GG Jr (2007) Handgrip strength predicts sexual behavior, body morphology, and aggression in male college students. Evol Hum Behav 28:423–429

    Article  Google Scholar 

  • Gobrogge KL, Breedlove SM, Klump KL (2008) Genetic and environmental influences on 2D:4D finger length ratios: a study of monozygotic and dizygotic male and female twins. Arch Sex Behav 37:112–118

    Article  PubMed  Google Scholar 

  • Green SB (1991) How many subjects does it take to do a regression analysis? Multivariate Behav Res 26:499–510

    Article  Google Scholar 

  • Guo G, Ou X-M, Roettger M, Shih JC (2008) The VNTR 2 repeat in MAOA and delinquent behavior in adolescence and young adulthood: associations and MAOA promoter activity. Eur J Hum Genet 16:626–634

    Article  PubMed  Google Scholar 

  • Haberstick BC, Lessem JM, Hopfer CJ, Smolen A, Ehringer MA, Timberlake D et al (2005) Monoamine oxidase A (MAOA) and antisocial behaviors in the presence of childhood and adolescent maltreatment. Am J Med Genet B Neuropsychiatr Genet 135:59–64

    Google Scholar 

  • Hampson E, Ellis CL, Tenk CM (2008) On the relation between 2D:4D and sex-dimorphic personality traits. Arch Sex Behav 37:133–144

    Article  PubMed  Google Scholar 

  • Harris JA (1997) A further evaluation of the aggression questionnaire: issues of validity and reliability. Behav Res Ther 35:1047–1053

    Article  PubMed  Google Scholar 

  • Heath EM, Morken NW, Campbell KA, Tkach D, Boyd EA, Strom DA (2001) Use of buccal cells collected in mouthwash as a source of DNA for clinical testing. Arch Pathol Lab Med 125:127–133

    PubMed  Google Scholar 

  • Hines M, Ahmed SF, Hughes IA (2003) Psychological outcomes and gender-related development in complete androgen insensitivity syndrome. Arch Sex Behav 32:93–101

    Article  PubMed  Google Scholar 

  • Kazemi-Esfarjani P, Trifiro MA, Pinsky L (1995) Evidence for a repressive function of the long polyglutamine tract in the human androgen receptor: possible pathogenetic relevance for the (CAG) n-expanded neuronopathies. Hum Mol Genet 4:523–527

    Article  PubMed  Google Scholar 

  • Krithivas K, Yurgalevitch SM, Mohr BA, Wilcox CJ, Batter SJ, Brown M, Longcope C, McKinlay JB, Kantoff PW (1999) Evidence that the CAG repeat in the androgen receptor gene is associated with the age-related decline in serum androgen levels in men. J Endocrinol 162:137–142

    Article  PubMed  Google Scholar 

  • Kuepper Y, Hennig J (2007) Behavioral aggression is associated with the 2D:4D ratio in men but not in women. J Individ Diff 28:64–72

    Article  Google Scholar 

  • La Spada AR, Wilson EM, Lubahn DB, Harding AE, Fischbeck KH (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352:77–79

    Article  PubMed  Google Scholar 

  • Latourelle SM, Elwess NL, Elwess JM (2008) Finger forecasting: a pointer to athletic prowess in women a preliminary investigation by an undergraduate biology class. Am Biol Teach 70:411–414

    Article  Google Scholar 

  • Lephart ED, Lund TD, Horvath TL (2001) Brain androgen and progesterone metabolizing enzymes: biosynthesis, distribution and function. Brain Res Rev 37:25–37

    Article  PubMed  Google Scholar 

  • Lindova J, Hruskova M, Pivonkova V, Kubena A, Flegr J (2008) Digit Ratio (2D:4D) and Cattell’s personality traits. Eur J Pers 22:347–356

    Article  Google Scholar 

  • Loehlin JC, Jonsson EG, Gustavsson JP, Schalling M, Medland SE, Montgomery GW, Martin NG (2004) Gender diagnosticity and androgen receptor gene CAG repeat sequence. Twin Res 7:456–461

    Article  PubMed  Google Scholar 

  • Lum A, Le Marchand L (1998) A simple mouthwash method for obtaining genomic DNA in molecular epidemiological studies. Cancer Epidemiol Biomarkers Prev 7:719–724

    PubMed  Google Scholar 

  • MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294–1303

    Article  PubMed  Google Scholar 

  • MacLusky NJ, Walters MJ, Clark AS, Toran-Allerand CD (1994) Aromatase in the central cortex, hippocampus, and mid-brain: ontogeny and developmental implications. Mol Cell Neurosci 5:691–698

    Article  PubMed  Google Scholar 

  • Malas MA, Dogan S, Evcil EH, Desdicioglu K (2006) Fetal development of the hand, digits and digit ratio (2D:4D). Early Hum Dev 82:469–475

    Article  PubMed  Google Scholar 

  • Manning JT (2002) Digit ratio: a pointer to fertility, behavior, and health. Rutgers University Press, New Brunswick, NJ

    Google Scholar 

  • Manning JT (2008) The finger ratio: sex, behaviour and disease revealed in the fingers. Faber and Faber, London

    Google Scholar 

  • Manning JT, Fink B (2008) Digit ratio (2D:4D), dominance, reproductive success, asymmetry, and sociosexuality in the BBC internet study. Am J Hum Biol 20:451–461

    Article  PubMed  Google Scholar 

  • Manning JT, Barley L, Walton J, Lewis-Jones D, Trivers RL, Singh D, Thornhill R, Rohde P, Bereckei T, Henzi P, Soler M, Sved A (2000) The 2nd:4th digit ratio, sexual dimorphism, population differences, and reproductive success: evidence for sexually antagonistic genes. Evol Hum Behav 21:163–183

    Article  PubMed  Google Scholar 

  • Manning JT, Bundred PE, Newton DJ, Flanagan BF (2003) The second to fourth digit ratio and variation in the androgen receptor gene. Evol Hum Behav 24:399–405

    Article  Google Scholar 

  • Manning JT, Stewart A, Bundred PE, Trivers RL (2004) Sex and ethnic differences in 2nd to 4th digit ratio of children. Early Hum Dev 80:161–168

    Article  PubMed  Google Scholar 

  • Mazur T (2005) Gender dysphoria and gender change in androgen insensitivity or micropenis. Arch Sex Behav 34:411–421

    Article  PubMed  Google Scholar 

  • Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21:353–397

    Article  PubMed  Google Scholar 

  • McDermott R, Tingley D, Cowden J, Frazzetto G, Johnson DDP (2009) Monoamine oxidase A gene (MAOA) predicts behavioral aggression following provocation. Proc Nat Acad Sci USA 106:2118–2123

    Article  PubMed  Google Scholar 

  • McIntyre MH (2006) The use of digit ratios as markers for perinatal androgen action. Reprod Biol Endocrinol 4:10

    Article  PubMed  Google Scholar 

  • McIntyre MH, Barrett ES, McDermott R, Johnson DDP, Cowden J, Rosen SP (2007) Finger length ratio (2D:4D) and sex differences in aggression during a simulated war game. Pers Individ Diff 42:755–764

    Article  Google Scholar 

  • Medland SE, Loehlin JC (2008) Multivariate genetic analyses of the 2D:4D ratio: examining the effects of hand and measurement technique in data from 757 twin families. Twin Res Hum Genet 11:335–341

    Article  PubMed  Google Scholar 

  • Medland SE, Zayats T, Glaser B, Nyholt DR, Gordon SD, Wright MJ, Montgomery GW, Campbell MJ, Henders AK, Timpson NJ, Peltonen L, Wolke D, Ring SM, Deloukas P, Martin NG, Smith GD, Evans DM (2010) A variant in LIN28B is associated with 2D:4D finger-length ratio, a putative retrospective biomarker of prenatal testosterone exposure. Am J Hum Genet 86:519–525

    Article  PubMed  Google Scholar 

  • Meyer-Lindenberg A, Buckholtz JW, Kolachana B, Hariri AR, Pezawas L, Blasi G, Wabnitz A, Honea R, Verchinski B, Callicott JH, Egan M, Mattay V, Weinberger DR (2006) Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Nat Acad Sci USA 103:6269–6274

    Article  PubMed  Google Scholar 

  • Moroschan G, Hurd PL, Nicoladis E (2009) Sex differences in the use of indirect aggression in adult Canadians. Evol Psychol 7:146–159

    Google Scholar 

  • Moser BK, Stevens GR (1992) Homogeneity of variance in the two-sample means test. Am Stat 46:19–21

    Article  Google Scholar 

  • Naftolin F, MacLusky N (1984) Aromatization hypothesis revisited. In: Serio M, Motta M, Zanisi M, Marini L (eds) Sexual differentiation: basic and clinical aspects, vol 11. Raven Press, New York, pp 79–91

  • Neave N (2008) Hormones and behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Paul SN, Kato BS, Cherkas LF, Andrew T, Spector TD (2006) Heritability of the second to fourth digit ratio (2D:4D): a twin study. Twin Res Hum Genet 9:215–219

    Article  PubMed  Google Scholar 

  • Putz DA, Gaulin SJC, Sporter RJ, McBurney DH (2004) Sex hormones and finger length. What does 2D:4D indicate? Evol Hum Behav 25:182–199

    Article  Google Scholar 

  • Raine A (2008) From genes to brain to antisocial behavior. Curr Dir Psychol Sci 17:323–328

    Article  Google Scholar 

  • Rajender S, Pandu G, Sharma JD, Gandhi KPC, Singh L, Thangaraj K (2008) Reduced CAG repeats length in androgen receptor gene is associated with violent criminal behavior. Int J Legal Med 122:367–372

    Article  PubMed  Google Scholar 

  • Ruxton GD (2006) The unequal variance t-test is an underused alternative to Student’s t-test and the Mann–Whitney U test. Behav Ecol 17:688–690

    Article  Google Scholar 

  • Ryan BC, Vandenbergh JG (2002) Intrauterine position effects. Neurosci Biobehav Rev 26:665–678

    Article  PubMed  Google Scholar 

  • Sabol SZ, Hu S, Hamer D (1998) A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet 103:273–279

    Article  PubMed  Google Scholar 

  • Smail PJ, Reyes FI, Winter JSD, Faiman C (1981) The fetal hormone environment and its effect on the morphogenesis of the genital system. In: Kogan SJ, Hafez ESE (eds) Pediatric andrology. Martinus Nijhoff, The Hague, pp 1–19

    Google Scholar 

  • Stanworth RD, Kapoor D, Channer KS, Jones TH (2007) Androgen receptor CAG repeat polymorphism is associated with serum testosterone levels, obesity and serum leptin in men with type 2 diabetes. Endocrin Abs 13:258

    Google Scholar 

  • Stanworth RD, Kapoor D, Channer KS, Jones TH (2008) Androgen receptor CAG repeat polymorphism is associated with serum testosterone levels, obesity and serum leptin in men with type 2 diabetes. Eur J Endocrinol 159:739–746

    Article  PubMed  Google Scholar 

  • Svare B, Kinsley CH, Mann MA, Broida J (1984) Infanticide: accounting for genetic variation in mice. Physiol Behav 33:137–152

    Article  PubMed  Google Scholar 

  • Van Pottelbergh I, Lumbroso S, Goemaere S, Sultan C, Kaufman JM (2001) Lack of influence of the androgen receptor gene CAG-repeat polymorphism on sex steroid status and bone metabolism in elderly men. Clin Endocrinol 55:659–666

    Article  Google Scholar 

  • Voracek M, Dressler SG (2009) Familial resemblance in 2D:4D. Am J Phys Anthropol 140:376–380

    Article  PubMed  Google Scholar 

  • Voracek M, Stieger S (2009) Replicated nil associations of digit ratio (2D:4D) and absolute finger lengths with implicit and explicit measures of aggression. Psicothema 21:382–389

    PubMed  Google Scholar 

  • Yu M-W, Cheng S-W, Lin M-W, Yang S-Y, Liaw Y-F, Chang H-C, Hsiao T-J, Lin S-M, Lee S-D, Chen P-J, Liu C-J, Chen C-J (2000) Androgen-receptor gene CAG repeats, plasma testosterone levels, and risk of hepatitis B-related hepatocellular carcinoma. J Natl Cancer Inst 92:2023–2028

    Article  PubMed  Google Scholar 

  • Zitzmann M, Nieschlag E (2003) The CAG repeat polymorphism within the androgen receptor gene and maleness. Int J Androl 26:76–83

    Article  PubMed  Google Scholar 

  • Zitzmann M, Gromoll J, von Eckardstein A, Nieschlag E (2003) The CAG repeat polymorphism in the androgen receptor gene modulates body fat mass and serum concentrations of leptin and insulin in men. Diabetologia 46:31–39

    PubMed  Google Scholar 

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Acknowledgments

The authors thank Bernie Crespi for generously hosting PLH’s sabbatical work in his lab, providing all equipment, materials, resources and advice required for the extractions and AR geneotyping, and to Tanja Schwander and Lisa Raeburn for their advice and assistance in the lab. Thanks also to Felix Breden and Julian Guttman and their labs for equipment. Thanks also to Shelagh Campbell and her lab for providing resources and equipment for MAO-A genotyping, and to Ran Zhuo for assistance in the lab. This manuscript benefited greatly from comments by Associate Editor Sarah Medland and two anonymous reviewers. This research was supported by an NSERC (Canada) Discovery Grants to PLH, Bernie Crespi, and Shelagh Campbell.

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Hurd, P.L., Vaillancourt, K.L. & Dinsdale, N.L. Aggression, Digit Ratio and Variation in Androgen Receptor and Monoamine Oxidase A Genes in Men. Behav Genet 41, 543–556 (2011). https://doi.org/10.1007/s10519-010-9404-7

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