Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T08:01:03.210Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential susceptibility to rearing environment depending on dopamine-related genes: New evidence and a meta-analysis

Published online by Cambridge University Press:  24 January 2011

Marian J. Bakermans-Kranenburg  and
Marinus H. van Ijzendoorn
Marian J. Bakermans-Kranenburg*
Affiliation:
Leiden University
Marinus H. van Ijzendoorn*
Affiliation:
Leiden University
*
Address correspondence and reprint requests to: Marian J. Bakermans-Kranenburg or Marinus H. van IJzendoorn, Centre for Child and Family Studies, Leiden University, P.O. Box 9555, Leiden 2300 RB, The Netherlands; E-mail: bakermans@fsw.leidenuniv.nl or vanijzen@fsw.leidenuniv.nl.
Address correspondence and reprint requests to: Marian J. Bakermans-Kranenburg or Marinus H. van IJzendoorn, Centre for Child and Family Studies, Leiden University, P.O. Box 9555, Leiden 2300 RB, The Netherlands; E-mail: bakermans@fsw.leidenuniv.nl or vanijzen@fsw.leidenuniv.nl.
Get access Rights & Permissions [Opens in a new window]

Abstract

In the current paper we present new empirical data and meta-analytic evidence for the role of dopamine-related genes as a susceptibility factor interacting with the rearing environment for better and for worse, that is, increasing children's susceptibility to both the adverse effects of unsupportive environments and the beneficial effects of supportive rearing. In Study 1 we examined the readiness of 91 7-year-old children to donate their money to a charity (UNICEF). We tested whether the association between attachment and donating behavior was moderated by the presence of the dopamine receptor D4 (DRD4) 7-repeat allele. The attachment story completion task was used to assess attachment as an index of the quality of the rearing environment. Children with secure attachment representations donated more but only if they had the DRD4 7-repeat allele. In Study 2 we present the results of a meta-analysis of gene–environment studies on children up to 10 years of age involving dopamine-related genes (dopamine receptor D2, DRD4, dopamine transporter). The cumulative negative effects of these “risk genes” and adverse rearing environments have been stressed, but potentially cumulative positive effects of these same genes interacting with positive rearing environments remained largely unnoticed. We examined the associations between negative and positive rearing environments and developmental outcomes as moderated by dopamine-related gene polymorphisms. Children with the less efficient dopamine-related genes did worse in negative environments than the comparisons without the “genetic risk,” but they also profited most from positive environments. Findings are discussed in light of evolutionary theory, and illustrated with some practical implications of differential susceptibility.

Type
Special Section Articles
Information
Development and Psychopathology , Volume 23 , Issue 1 , February 2011 , pp. 39 - 52
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aron, E. N., & Aron, A. (1997). Sensory-processing sensitivity and its relation to introversion and emotionality. Journal of Personality and Social Psychology, 73, 345–368.CrossRefGoogle ScholarPubMed
Bachner-Melman, R., Gritsenko, I., Nemanov, L., Zohar, A. H., Dina, C., & Ebstein, R. P. (2005). Dopaminergic polymorphisms associated with selfreport measures of human altruism: A fresh phenotype for the dopamine D4 receptor. Molecular Psychiatry, 10, 333–335.CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2006). Gene–environment interaction of the dopamine D4 receptor (DRD4) and observed maternal insensitivity predicting externalizing behavior in preschoolers. Developmental Psychobiology, 48, 406–409.CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Genetic vulnerability or differential susceptibility in child development: The case of attachment. Journal of Child Psychology and Psychiatry, 48, 1160–1173.CrossRefGoogle ScholarPubMed
Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Pijlman, F. T. A., Mesman, J., & Juffer, F. (2008). Experimental evidence for differential susceptibility: Dopamine D4 receptor polymorphism (DRD4 VNTR) moderates intervention effects on toddlers' externalizing behavior in a randomized control trial. Developmental Psychology, 44, 293–300.CrossRefGoogle Scholar
Barr, C. L., & Kidd, K. K. (1993). Population frequencies of the A1 allele at the dopamine D2 receptor locus. Biological Psychiatry, 34, 204–209.CrossRefGoogle ScholarPubMed
Belsky, J. (1997). Variation in susceptibility to environmental influence: An evolutionary argument. Psychological Inquiry, 8, 182–185.CrossRefGoogle Scholar
Belsky, J., Bakermans-Kranenbug, M. J., & van IJzendoorn, M. H. (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16, 300–304.CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis–stress: Differential susceptibility to environmental influence. Psychological Bulletin, 135, 885–908.CrossRefGoogle Scholar
Berman, S., Ozkaragoz, T., Young, R. M., & Noble, E. P. (2002). D2 dopamine receptor gene polymorphism discriminates two kinds of novelty seeking. Personality and Individual Differences, 33, 867–882.CrossRefGoogle Scholar
Blair, C. (2002). Early intervention for low birth weight preterm infants: The role of negative emotionality in the specification of effects. Development and Psychopathology, 14, 311–332.CrossRefGoogle ScholarPubMed
Borenstein, M., Hedges, L. V., & Higgins, J. P. T. (2009) Introduction to meta-analysis. Chichester: Wiley.Google Scholar
Bowles, S. (2008). Being human: Conflict: Altruism's midwife. Nature, 456, 326–328.CrossRefGoogle Scholar
Boyce, W. T., Chesney, M., Alkon, A., Tschann, J. M., Adams, S., Chesterman, B., et al. (1995). Psychobiologic reactivity to stress and childhood respiratory illnesses: Results of two prospective studies. Psychosomatic Medicine, 57, 411–422.CrossRefGoogle ScholarPubMed
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and function of stress reactivity. Development and Psychopathology, 17, 271–301.CrossRefGoogle ScholarPubMed
Bretherton, I., Prentiss, C., & Ridgeway, D. (1990). Family relationships as represented in a story-completion task at thirty-seven and fifty-four months of age. New Directions for Child and Adolescent Development, 48, 85–105.CrossRefGoogle Scholar
Bronfenbrenner, U. (1979). The ecology of human development: Experiments by nature and design. Cambridge, MA: Harvard University Press.Google Scholar
Carlson, E. A. (1998). A prospective longitudinal study of attachment disorganization/disorientation. Child Development, 69, 1107–1128.CrossRefGoogle ScholarPubMed
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., et al. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851–854.CrossRefGoogle ScholarPubMed
Cassidy, J. (1988). Child mother attachment and the self in six year olds. Child Development, 59, 121–134.CrossRefGoogle ScholarPubMed
Congdon, E., Lesch, K. P., & Canli, T. (2008); Analysis of DRD4 and DAT polymorphisms and behavioral inhibition in healthy adults: Implications for impulsivity. American Journal of Medical Genetics, 147B, 27–32.Google ScholarPubMed
Darwin, C. (1982). The descent of man, and selection in relation to sex. Princeton, NJ: Princeton University Press. [Original work published 1871]Google Scholar
Deater-Deckard, K., Dodge, K. A., Bates, J. E., & Pettit, G. S. (1996). Discipline among African American and European American mothers: Links to children's externalizing behaviors. Developmental Psychology, 32, 1065–1072.CrossRefGoogle Scholar
De Waal, F. B. M. (2008). Putting the altruism back into altruism: The evolution of empathy. Annual Review of Psychology, 59, 279–300.CrossRefGoogle ScholarPubMed
Ding, Y. C., Chi, H. C., Grady, D. L., Morishima, A., Kidd, J. R., Kidd, K. K., et al. (2002). Evidence of positive selection acting at the human dopamine receptor D4 gene locus. Proceedings of the National Academy of Sciences of the United States of America, 99, 309–314.CrossRefGoogle ScholarPubMed
Ebstein, R. P., Israel, S., Chew, S. H., Zhong, S., & Knafo, A. (2010). Genetics of human social behavior. Neuron, 65, 831–844,CrossRefGoogle ScholarPubMed
Eisenberg, D. T. A., Campbell, B., Gray, P. B., & Sorenson, M. D. (2008). Dopamine receptor genetic polymorphisms and body composition in undernourished pastoralists: An exploration of nutrition indices among nomadic and recently settled Ariaal men of northern Kenya. BMC Evolutionary Biology, 8, 173.CrossRefGoogle ScholarPubMed
Eisenberg, N., Guthrie, I. K., Murphy, B. C., Shepard, S. A., Cumberland, A., & Carlo, G. (1999). Consistency and development of prosocial dispositions: A longitudinal study. Child Development, 70, 1360–1372.CrossRefGoogle ScholarPubMed
Eisenberg, N., Shell, R., Pasternack, J., Lennon, R., Beller, R., & Mathy, R. M. (1987). Prosocial development in middle childhood: A longitudinal study. Developmental Psychology, 23, 712–718.CrossRefGoogle Scholar
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 7–28.CrossRefGoogle Scholar
Espy, K. A. & Cwik, M. F. (2004). The development of a Trail Making Test in young children: The Trails-P. Clinical Neuropsychologist, 18, 411–422.CrossRefGoogle ScholarPubMed
Evans, D. E. & Rothbart, M. K. (2007). Developing a model for adult temperament. Journal of Research in Personality, 41, 868–888.CrossRefGoogle Scholar
Faraone, S. V., Perlis, R. H., Doyle, A. E., Smoller, J. W., Goralnick, J. J., Holmgren, M. A., et al. 2005. Molecular genetics of attention-deficit/hyperactivity disorder. Biological Psychiatry, 57, 1313–1323.CrossRefGoogle ScholarPubMed
Fearon, R. M. P., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Lapsley, A., & Roisman, G. I. (2010). The significance of insecure attachment and disorganization in the development of children's externalizing behavior: A meta-analytic study. Child Development, 81, 435–456.CrossRefGoogle ScholarPubMed
Fox, N. A., Hane, A. A., & Pine, D. S. (2007). Plasticity for affective neurocircuitry. How the environment affects gene expression. Current Directions in Psychological Science, 16, 1–5.CrossRefGoogle Scholar
Froehlich, T. E., Lanphear, B. P., Dietrich, K. N., Cory-Slechta, D. A., Wang, N., & Kahn, R. S. (2007). Interactive effects of a DRD4 polymorphism, lead, and sex on executive functions in children. Biological Psychiatry, 62, 243–249.CrossRefGoogle ScholarPubMed
Gervai, J., Novak, A., Lakatos, K., Toth, I., Danis, I., Ronai, Z., et al. (2007). Infant genotype may moderate sensitivity to maternal affective communications: Attachment disorganization, quality of care, and the DRD4 polymorphism. Social Neuroscience, 2, 307–319.Google ScholarPubMed
Gilissen, R., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., & Van der Veer, R. (2008). Parent–child relationship, temperament, and physiological reactions to fear-inducing film clips: Further evidence for differential susceptibility. Journal of Experimental Child Psychology, 99, 182–195.CrossRefGoogle ScholarPubMed
Goldstein, H., & Healy, M. J. R. (1995). The graphical presentation of a collection of means, Journal of the Royal Statistical Society, 158A, 175–177.CrossRefGoogle Scholar
Grunberg, N. E., Maycock, V. A., & Anthony, B. J. (1985). Material altruism in children. Basic and Applied Social Psychology, 6, 1–11.CrossRefGoogle Scholar
Hesse, E. (2008). The Adult Attachment Interview: Protocol, method of analysis, and empirical studies. In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research, and clinical applications (pp. 552–598). New York: Guilford Press.Google Scholar
Hoffman, M. L. (1984). Interaction of affect and cognition in empathy. In Izard, C. E., Kagan, J., & Zajone, R. B. (Eds.), Emotions, cognitions, and behavior (pp. 103–131). Cambridge: Cambridge University Press.Google Scholar
Hrdy, S. B. (2009). Mothers and others: The evolutionary origins of mutual understanding. Cambridge, MA: Harvard University Press.Google Scholar
Kaffman, A., & Meaney, M. J. (2007). Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry, 48, 224–244.CrossRefGoogle ScholarPubMed
Kahn, R. S., Khoury, J., Nichols, W. C., & Lanphear, B. P. (2003). Role of dopamine transporter genotype and maternal prenatal smoking in childhood hyperactive–impulsive, inattentive, and oppositional behaviors. Journal of Pediatrics, 143, 104–110.CrossRefGoogle ScholarPubMed
Kim-Cohen, J., Caspi, A., Taylor, A., Williams, B., Newcombe, R., Craig, I. W., et al. (2006). MAOA, maltreatment, and gene–environment interaction predicting children's mental health: New evidence and a meta-analysis. Molecular Psychiatry, 11, 903–913.CrossRefGoogle ScholarPubMed
Klein, T. A., Neumann, J., Reuter, M., Hennig, J., Von Cramon, D. Y., & Ullsperger, M. (2007). Genetically determined learning from errors. Science, 318, 1642–1645.CrossRefGoogle ScholarPubMed
Klein Velderman, M., Bakermans-Kranenburg, M. J., Juffer, F., & van IJzendoorn, M. H. (2006). Effects of attachment-based interventions on maternal sensitivity and infant attachment: Differential susceptibility of highly reactive infants. Journal of Family Psychology, 20, 266–274.CrossRefGoogle ScholarPubMed
Knafo, A. (2009). Prosocial development: The intertwined roles of children's genetics and their parental environment. Paper presented at the Biennial Meeting of the Society for Research in Child Development, Denver, CO, April 2–4.Google Scholar
Knafo, A., Zahn-Waxler, C., Van Hulle, C., Robinson, J. L., & Rhee, S. H. (2008). The developmental origins of a disposition towards empathy: Genetic and environmental contributions. Emotion, 8, 737–752.CrossRefGoogle Scholar
Kochanska, G., Askan, N., & Joy, M. E. (2007). Children's fearfulness as a moderator of parenting in early socialization: Two longitudinal studies. Developmental Psychology, 43, 222–237.CrossRefGoogle ScholarPubMed
Krevans, J., & Gibbs, J. C. (1996). Parents' use of inductive discipline: Relations to children's empathy and prosocial behavior. Child Development, 67, 3263–3277.CrossRefGoogle ScholarPubMed
Levitan, R. D., Masellis, M., Basile, V. S., Lam, R. W., Kaplan, A. S., Davis, C., et al. (2004). The dopamine-4 receptor gene associated with binge eating and weight gain in women with seasonal affective disorder: An evolutionary perspective. Biological Psychiatry, 56, 665–669.CrossRefGoogle ScholarPubMed
Li, Y., Shao, C., Zhang, D., Zhao, M.Lin, L., Yan, P., et al. (2006). The effect of dopamine D2, D5 receptor and transporter (SLC6A3) polymorphisms on the cue-elicited heroin craving in Chinese. American Journal of Medical Genetics, 141B, 269–273.Google ScholarPubMed
Maher, B. S., Marazita, M. L., Ferrell, R. E., & Vanyukov, M. M. 2002. Dopamine system genes and attention deficit hyperactivity disorder: A meta-analysis. Psychiatric Genetics 12, 207–215.CrossRefGoogle ScholarPubMed
Mikulincer, M., & Shaver, P. R. (2008). “Can't buy me love”: An attachment perspective on social support and money as psychological buffers. Psychological Inquiry, 19, 167–173.CrossRefGoogle Scholar
Noble, E. P. (2003). D2 dopamine receptor gene in psychiatric and neurological disorders and its phenotypes. American Journal of Medical Genetics, 116B, 103–125.Google ScholarPubMed
Posner, M. I., & Rothbart, M. K. (2007). Research on attention networks as a model for the integration of psychological science. Annual Review of Psychology, 58, 1–23.CrossRefGoogle Scholar
Propper, C., Willoughby, M., Halpern, C. T., Cox, M., & Carbone, M. A. (2007). Parenting quality, DRD4, and the prediction of externalizing and internalizing behaviors in early childhood. Developmental Psychobiology, 49, 619–632.CrossRefGoogle ScholarPubMed
Richters, J. E., & Waters, E. (1992). Attachment and socialization: The positive side of social influence. In Lewis, M. & Feinman, S. (Eds.), Social influences and behavior. New York: Plenum Press.Google Scholar
Robbins, T. W., & Everitt, B. J. (1999). Motivation and reward. In Bloom, F. E., Landis, S. C., Robert, J. L., Squire, L. R., & Zigmond, M. J. (Eds.), Fundamental neuroscience (pp. 1246–1260). San Diego, CA: Academic Press.Google Scholar
Rushton, J. P., Littlefield, C. H., & Lumsden, C. J. (1986). Gene culture coevolution of complex social behavior: Human altruism and mate choice. Proceedings of the National Academy of Sciences of the United States of America, 83, 7340–7343.CrossRefGoogle ScholarPubMed
Rushton, J. P., & Wheelwright, M. (1980). Validation of donating to charity as a measure of children's altruism. Psychological Reports, 47, 803–806.CrossRefGoogle Scholar
Rutter, M. (2006). Genes and Behavior. Nature–nurture interplay explained. Oxford: Blackwell.Google Scholar
Rutter, M. (2007). Gene–environment interdependence. Developmental Science, 10, 12–18.CrossRefGoogle ScholarPubMed
Sheese, B. E., Voelker, P. M., Rothbart, M. K., & Posner, M. I. (2007). Parenting quality interacts with genetic variation in dopamine receptor D4 to influence temperament in early childhood. Development and Psychopathology, 19, 1039–1046.CrossRefGoogle ScholarPubMed
Spiecker, B. (1991). Emoties en morele opvoeding [Emotions and moral education]. Meppel, The Netherlands: Boom.Google Scholar
Suomi, S. (1997). Early determinants of behaviour. British Medical Bulletin, 53, 170–184.CrossRefGoogle ScholarPubMed
Swanson, J., Flodman, P., Kennedy, J., Spence, M. A., Moyzis, R., Schuck, S., et al. (2000). Dopamine genes and ADHD. Neuroscience and Biobehavioral Reviews, 24, 21–25.CrossRefGoogle ScholarPubMed
Tabachnik, B. G., & Fidell, L. S. (2006). Using multivariate statistics. Boston: Allyn & Bacon.Google Scholar
Tripp, G., & Wickens, J. R. (2008). Dopamine transfer deficit: A neurobiological theory of altered reinforcement mechanisms in ADHD. Journal of Child Psychology and Psychiatry, 49, 691–704.CrossRefGoogle ScholarPubMed
Van IJzendoorn, M. H. (1997). Attachment, emergent morality, and aggression: Toward a developmental socioemotional model of antisocial behavior. International Journal of Behavioral Development, 21, 703–727.CrossRefGoogle Scholar
Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., & Mesman, J. (2008). Dopamine system genes associated with parenting in the context of daily hassles. Genes, Brain and Behavior, 7, 403–410.CrossRefGoogle ScholarPubMed
Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Pannebakker, F., & Out, D. (2010). In defense of situational morality: Genetic, dispositional and situational determinants of children's donating to charity. Journal of Moral Education, 39, 1–20.CrossRefGoogle Scholar
Van IJzendoorn, M. H., Caspers, K., Bakermans-Kranenburg, M. J., Beach, S. R. H., & Philibert, R. (2010). Methylation matters: Interaction between methylation density and 5HTT genotype predicts unresolved loss or trauma. Biological Psychiatry, 68, 405–407.CrossRefGoogle ScholarPubMed
Van IJzendoorn, M. H., Juffer, F., & Klein Poelhuis, C. W. (2005). Adoption and cognitive development: A meta-analytic comparison of adopted and nonadopted children's IQ and school performance. Psychological Bulletin, 131, 301–316.CrossRefGoogle ScholarPubMed
Verschueren, K., & Marcoen, A. (1994). Test met gehechtheidsverhalen classificatiesysteem: Aanpassing van de Doll Stories Completion Task van Cassidy (1986) [Adaptation of the Doll Stories Completion Task of Cassidy (1986)]. Unpublished manuscript, Katholieke Universiteit Leuven, Center for Developmental Psychology.Google Scholar
Verschueren, K., & Marcoen, A. (1999). Representation of self and socioemotional competence in kindergartners: Differential and combined effects of attachment to mother and father. Child Development, 70, 183–201.CrossRefGoogle Scholar
Volbrecht, M. M., Lemery-Chalfant, K., Akzan, N., Zahn-Waxler, C., & Goldsmith, H. H. (2007). Examining the familial link between positive effect and empathy development in the second year. Journal of Genetic Psychology, 168, 105–130.CrossRefGoogle Scholar
Wachs, T. D. (1983). The use and abuse of environment in behavior–genetic research. Child Development, 54, 396–407.CrossRefGoogle ScholarPubMed
Wachs, T. D. (1991). Synthesis: Promising research designs, measures, and strategies. In Wachs, T. D. & Plomin, R. (Eds.), Conceptualization and measurement of organism–environment interaction (pp. 162–182). Washington, DC: American Psychological Association.CrossRefGoogle Scholar
Waldman, I. D. (2007). Gene–environment interactions reexamined: Does mother's marital stability interact with the dopamine D2 gene in the etiology of childhood attention-deficit/hyperactivity disorder? Development and Psychopathology, 19, 1117–1128.CrossRefGoogle ScholarPubMed
Wang, E. T., Ding, Y.-C., Flodman, P., Kidd, J. R., Kidd, K. K., Grady, D. L., et al. (2004). The genetic architecture of selection at the human dopamine receptor D4 (DRD4) gene locus. American Journal of Human Genetics, 74, 931–944.CrossRefGoogle ScholarPubMed
Wiebe, S. A., Espy, K. A., Stopp, C., Respass, J., Stewart, P., Jameson, T. R., et al. (2009). Gene–environment interactions across development: Exploring DRD2 genotype and prenatal smoking effects on self-regulation. Developmental Psychology, 45, 31–44.CrossRefGoogle ScholarPubMed
Williams, R. B., Marchuk, D. A., Gadde, K. M., Barefoot, J. C., Crichnik, K., Helms, M. J., et al. (2003). Serotonin-related gene polymorphisms and central nervous system serotonin function. Neuropsychopharmacology, 28, 533–541.CrossRefGoogle ScholarPubMed
Wolf, M., Van Doorn, G. S., & Weissing, F. J. (2008). Evolutionary emergence of responsive and unresponsive personalities. Proceedings of the National Academy of Sciences of the United States of America, 105, 15825–15830.CrossRefGoogle ScholarPubMed