Skip to main content Accessibility help

Heritability of children's prosocial behavior and differential susceptibility to parenting by variation in the dopamine receptor D4 gene

  • Ariel Knafo (a1), Salomon Israel (a2) and Richard P. Ebstein (a1) (a2)


Theoretical considerations and new empirical evidence suggest that children's development cannot simply be explained by either genes or environment but that their interaction is important to understanding child behavior. In particular, a genetic polymorphism, the exon III repeat region of the dopamine receptor D4, has been the focus of interest regarding differential susceptibility to parental influence. To study environmental and genetic influences on children's prosocial behavior, 168 twin pairs (mean age = 44 months) participated in an experiment that assessed prosocial behavior via three measures: compliant prosocial behavior elicited in response to social requests, self-initiated prosocial behavior enacted voluntarily, and mothers' rating of children's behavior. Genetic effects accounted for 34% to 53% of the variance in prosocial behavior. The rest of the variance was accounted for by nonshared environment and error. Parenting measures of maternal positivity, negativity, and unexplained punishment did not correlate significantly with children's prosocial behavior. However, when parenting was stratified by presence or absence of the child's dopamine receptor D4 7-repeat allele in an overlapping sample of 167 children to model differential susceptibility to parental influence, a richer picture emerged. Positive parenting related meaningfully to mother-rated prosocial behavior, and unexplained punishment related positively to self-initiated prosocial behavior, but only among children carrying the 7-repeat allele. The findings demonstrate that a molecular genetic strategy, based on genotyping of common polymorphisms and combined with a classic twin approach, provides a richer description of how genes and environment interact to shape children's behavior, and allows for the identification of differential sensitivity to parental influence.


Corresponding author

Address correspondence and reprint requests to: Ariel Knafo, Psychology Department, Hebrew University of Jerusalem, Mount Scopus, Jerusalem 91905, Israel; E-mail:


Hide All
Asbury, K., Dunn, J. F., Pike, A., & Plomin, R. (2003). Nonshared environmental influences on individual differences in early behavioral development: A monozygotic twin differences study. Child Development, 74, 933943.
Asghari, V., Sanyal, S., Buchwalt, S., Paterson, A., Jovanovic, V., & Van Tol, H. H. (1995). Modulation of intracellular cyclic AMP levels by different human dopamine D4 receptor variants. Journal of Neurochemistry, 65, 11571165.
Bachner-Melman, R., Gritsenko, I., Nemanov, L., Zohar, A. H., & Ebstein, R. P. (2005). Dopaminergic polymorphisms associated with self-report measures of human altruism: A fresh phenotype for the dopamine D4 receptor. Molecular Psychiatry, 10, 333335.
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, 406409.
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Research review: Genetic vulnerability or differential susceptibility in child development: The case of attachment. Journal of Child Psychology and Psychiatry, 48, 11601173.
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2009). Differential susceptibility to rearing environment depending on dopamine-related genes: Children's donating to UNICEF. Paper presented at the Society for Research in Child Development Meeting, Denver, CO.
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 controlled trial. Developmental Psychology, 44, 293300.
Bar-Tal, D. (1982). Sequential development of helping behavior: A cognitive–learning approach. Developmental Review, 2, 101124.
Batson, C. D. (2009). Empathy-induced altruistic motivation. In Shaver, P. R. & Mikulincer, M. (Eds.), Prosocial motives, emotions, and behavior (pp. 1534). Washington DC: American Psychological Association.
Belsky, J. (1997). Variation in susceptibility to environmental influence: An evolutionary argument. Psychological Inquiry, 8, 182186.
Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16, 300304.
Belsky, J., Hsieh, K., & Crnic, K. (1998). Mothering, fathering, and infant negativity as antecedents of boys' externalizing problems and inhibition at age 3 years: Differential susceptibility to rearing experience? Development and Psychopathology, 10, 301319.
Belsky, J., & Pluess, M. (2009a). The Nature (and nurture?) of plasticity in early human development. Perspectives on Psychological Science, 4, 345351.
Belsky, J., & Pluess, M. (2009b). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908.
Benenson, J. F., Pascoe, J., & Radmore, N. (2007). Children's altruistic behavior in the dictator game. Evolution and Human Behavior, 28, 168175.
Benish-Weisman, M., Steinberg, T., & Knafo, A. (2010). Genetic and environmental links between children's temperament and their problems with peers. Israel Journal of Psychiatry, 47, 144151.
Benjamin, J., Li, L., Patterson, C., Greenberg, B. D., Murphy, D. L., & Hamer, D. H. (1996). Population and familial association between the D4 dopamine receptor gene and measures of Novelty Seeking. Nature Genetics, 12, 8184.
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, 411422.
Boyce, W. T., &, Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity, Development and Psychopathology, 17, 271301.
Burt, S. A. (2008). Genes and popularity: Evidence of an evocative gene–environment correlation. Psychological Science, 19, 112113.
Canli, T. (2008). Toward a “molecular psychology” of personality. In John, O. P., Robins, R. W., & Pervin, L. A. (Eds.). Handbook of personality: Theory and research (pp. 311327). New York: Guilford Press.
Carlo, G., Roesch, S. C., & Melby, J. (1998). The multiplicative relations of parenting and temperament to prosocial and antisocial behaviors in adolescence. Journal of Early Adolescence, 18, 266290.
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, W. I., et al. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851854.
Caspi, A., Moffitt, T. E., Morgan, J., Rutter, M., Taylor, A., Arseneault, L., et al. (2004). Maternal expressed emotion predicts children's antisocial behavior problems: Using monozygotic-twin differences to identify environmental effects on behavioral development. Developmental Psychology, 40, 149161.
Cesarini, D., Dawes, C. T., Johannesson, M., Lichtenstein, P., & Wallace, B. (2009). Experimental game theory and behavior genetics. Annals of the New York Academy of Sciences, 1167, 6675.
Cicchetti, D., & Dawson, G. (2002). Multiple levels of analysis [Editorial]. Development and Psychopathology, 14, 417420.
Clark, K. E., & Ladd, G. W. (2000). Connectedness and autonomy support in parent–child relationships: Links to children's socioemotional orientation and peer relationships. Developmental Psychology, 36, 485498.
David, S. P., & Munafo, M. R. (2008). Genetic variation in the dopamine pathway and smoking cessation. Pharmacogenomics, 9, 13071321.
DeCoster, J. (2007). Applied linear regression notes set 1. Retrieved March 3, 2005, from
De Waal, F. B. M. (2008). Putting the altruism back into altruism: The evolution of empathy. Annual Review of Psychology, 59, 279300.
DiLalla, L. F., Elam, K. K., & Smolen, A. (2009). Genetic and gene–environment interaction effects on preschoolers' social behaviors. Developmental Psychobiology, 51, 451464.
Durston, S., Fossella, J. A., Casey, B. J., Hulshoff Pol, H. E., Galvan, A., Schnack, H. G., et al. (2005). Differential effects of DRD4 and DAT1 genotype on fronto-striatal gray matter volumes in a sample of subjects with attention deficit hyperactivity disorder, their unaffected siblings, and controls. Molecular Psychiatry, 10, 678685.
Ebstein, R. P., Novick, O., Umansky, R., Priel, B., Osher, Y., Blaine, D., et al. (1996). Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of Novelty Seeking. Nature Genetics, 12, 7880.
Eisenberg, N. (2004). The early development of prosocial tendencies. In Leavitt, L. A. & Hall, D. M. B. (Eds.), Social and moral development: Emerging evidence on the toddler years. New Brunswick, NJ: Johnson & Johnson Pediatric Institute, L.L.C.
Eisenberg, N., Cameron, E., & Tryon, F. (1984). Prosocial behavior in the preschool years: Methodological and conceptual issues. In Staub, E., Bar-Tal, D., Karylowski, J., & Reykowski, J. (Eds.), The development and maintenance of prosocial behavior: International perspectives on positive development (pp. 101115). New York: Plenum Press.
Eisenberg, N., Fabes, R. A., & Spinrad, T. (2006). Prosocial development. In Eisenberg, N. (Vol. Ed.) & Damon, W. & Lerner, R. M. (Series Eds.), Handbook of child psychology: Vol. 3. Social, emotional, and personality development (6th ed., pp. 646718). Hoboken, NJ: Wiley.
Eisenberg, N., Pasternack, J. F., Cameron, E., & Tryon, K. (1984). The relation of quantity and mode of prosocial behavior to moral cognitions and social style. Child Development, 55, 14791485.
Eisenberg, N., Wolchik, S. A., Goldberg, L., & Engel, I. (1992). Parental values, reinforcement, and young children's prosocial behavior: A longitudinal study. Journal of Genetic Psychology, 153, 1936.
Ellis, J., & Boyce, T. (2008). Biological sensitivity to context. Current Directions in Psychological Science, 17, 183187.
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, 728.
Fan, J., Fossella, J., Sommer, T., Wu, Y., & Posner, M. I. (2003). Mapping the genetic variation of executive attention onto brain activity. Proceedings of the National Academy of Sciences of the United States of America, 100, 74067411.
Gervai, J., Nemoda, Z., Lakatos, K., Ronai, Z., Toth, I., Ney, K., et al. (2005). Transmission disequilibrium tests confirm the link between DRD4 gene polymorphism and infant attachment. American Journal of Medical Genetics, 132B, 126130.
Gillespie, N. A., Cloninger, C. R., Heath, A. C., & Martin, N. G. (2003). The genetic and environmental relationship between Cloninger's dimensions of temperament and character. Personality and Individual Differences, 35, 19311946.
Goodman, R. (1997). The Strengths and Difficulties Questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38, 581586.
Gregory, A. M., Light-Häusermann, J. H., Rijsdijk, F., & Eley, T. C. (2009). Behavioral genetic analyses of prosocial behavior in adolescents. Developmental Science, 12, 165174.
Grusec, J. E. (1991). Socializing concern for others in the home. Developmental Psychology, 27, 338342.
Grusec, J. E., & Davidov, M. (2010). Integrating different perspectives on socialization theory and research: A domain-specific approach. Child Development, 81, 687709.
Hartmann, D. P., Gelfand, D. M., Smith, C. L., Paul, S. C., Cromer, C. C., Page, B. C., et al. (1976). Factors affecting the acquisition and elimination of children's donating behavior. Journal of Experimental Child Psychology, 21, 328338.
Hastings, P. D., Utendale, W. T., & Sullivan, C. (2007). The socialization of prosocial development. In Grusec, J. E. & Hastings, P. D. (Eds.), Handbook of socialization (pp. 638664). New York: Guilford Press.
Hoffman, M. L. (1970). Moral development. In Mussen, P. H. (Ed.), Carmichael's manual of child development (Vol. 2, pp. 261359), New York: Wiley.
Hoffman, M. L. (1988). Moral development. In Bornstein, M. & Lamb, M. (Eds.), Developmental psychology: An advanced textbook (pp. 497548). Hillsdale, NJ: Erlbaum.
Hur, Y. M., & Rushton, J. P. (2007). Genetic and environmental contributions to prosocial behaviour in 2- to 9-year-old South Korean twins. Biology Letters, 3, 664666.
Iannotti, R. J. (1985). Naturalistic and structured assessments of prosocial behavior in preschool children: The influence of empathy and perspective taking. Developmental Psychology, 21, 4655.
Insel, T.R. (2003). Is social attachment an addictive disorder? Physiology & Behavior, 79, 351357.
Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Reibold, M., Bachner-Melman, R., et al. (2008). Molecular genetic studies of the arginine vasopressin 1a receptor (AVPR1a) and the oxytocin receptor (OXTR) in human behavior: From autism to altruism with some notes in between. Progress in Brain Research, 170, 435449.
Israel, S., Lerer, E., Shalev, I.,, Uzefovsky, F., Riebold, M., Laiba, E., et al. (2009). The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task. PLoS ONE, 4, e5535.
Jaffee, S. R., & Price, T. S. (2007). Gene–environment correlations: A review of the evidence and implications for prevention of mental illness. Molecular Psychiatry, 12, 432442.
Kan, K., Ploeger, A., Raijmakers, M. E. J., Dolan, C. V., & van der Maas, H. L. J. (2010). Nonlinear epigenetic variance: Review and simulations. Developmental Science, 13, 1127.
Knafo, A. (2006). The Longitudinal Israeli Study of Twins (LIST): Children's social development as influenced by genetics, abilities, and socialization. Twin Research and Human Genetics, 9, 791798.
Knafo, A., & Israel, S. (2009). Genetic and environmental influences on prosocial behavior. In Mikulincer, M. & Shaver, P. R. (Eds.), Prosocial motives, emotions, and behavior: The better angels of our nature (pp. 149167). Washington, DC: American Psychological Association.
Knafo, A., Israel, S., Darvasi, A., Bachner-Melman, R., Uzefovsky, F., Cohen, L., et al. (2008). Individual differences in allocation of funds in the Dictator Game and postmortem hippocampal mRNA levels are correlated with length of the arginine vasopressin 1a receptor (AVPR1a) RS3 promoter-region repeat. Genes, Brain and Behavior, 7, 266275.
Knafo, A., & Plomin, R. (2006a). Parental discipline and affection, and children's prosocial behavior: Genetic and environmental links. Journal of Personality and Social Psychology, 90, 147164.
Knafo, A., & Plomin, R. (2006b). Prosocial behavior from early to middle childhood: Genetic and environmental influences on stability and change. Developmental Psychology, 42, 771786.
Knafo, A., & Schwartz, S. H. (2003). Parenting and adolescents' accuracy in perceiving parental values. Child Development, 73, 595611.
Knafo, A., Steinberg, T., & Goldner, I. (in press). Children's low affective perspective-taking ability is associated with low self-initiated prosociality. Emotion.
Knafo, A., & Uzefovsky, F. (in press). Variation in empathy: The interplay of genetic and environmental factors. In Legerstee, M., Haley, D. W., & Bornstein, M. H. (Eds.). The developing infant mind: Integrating biology and experience. New York: Guilford Press.
Knafo, A., Zahn-Waxler, C., Davidov, M., Van Hulle, C., Robinson, J., & Rhee, S. H. (2009). Empathy in early childhood: Genetic, environmental and affective contributions. Annals of the New York Academy of Sciences, 1167, 103114.
Knafo, A., Zahn-Waxler, C., Van Hulle, C., Robinson, J. L., Rhee, S. H. (2008). The developmental origins of a disposition toward empathy: Genetic and environmental contributions. Emotion, 8, 737752.
Kochanska, G. (1995). Children's temperament, mothers' discipline, and security of attachment: Multiple pathways to emerging internalization. Child Development, 66, 597615.
Krevans, J., & Gibbs, J. C. (1996). Parents' use of inductive discipline: Relations to children's empathy and prosocial behavior. Child Development, 67, 32633277.
Laucht, M., Becker, J., & Schmidt, M. H. (2006). Visual exploratory behaviour in infancy and novelty seeking in adolescence: Two developmentally specific phenotypes of ADHD. Journal of Child Psychology and Psychiatry, 47, 11431151.
Locke, L. M., & Prinz, R. J. (2002). Measurement of parental discipline and nurturance. Clinical Psychology Review, 22, 895929.
McClernon, F. J., Hutchison, K. E., Rose, J. E. & Kozink, R. V. (2007). DRD4 VNTR polymorphism is associated with transient fMRI-BOLD responses to smoking cues. Psychopharmacology, 194, 433441.
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12, 342348.
Miller, P. A., Eisenberg, N., Fabes, R. A., Shell, R., & Gular, S. (1989). Socialization of empathic and sympathetic responding. In Eisenberg, N. (Ed.), The development of empathy and related vicarious responses: New Directions in child development (pp. 6583). San Francisco, CA: Jossey–Bass.
Munafò, M. R., Yalcin, B., Willis-Owen, S. A., & Flint, J. (2008). Association of the dopamine D4 receptor (DRD4) gene and approach-related personality traits: Meta-analysis and new data. Biological Psychiatry, 63, 197206.
Neale, M. C., Boker, S. M., Xie, G., & Maes, H. H. (1999). Mx: Statistical modeling (5th ed.) [Computer software]. Richmond, VA: Virginia Commonwealth University, Department of Psychiatry.
Oakley, B., Knafo, A., Madhavan, G., & Wilson, D. S. (Eds.). (in press). Pathological altruism. New York: Oxford University Press.
Oakley, B., Knafo, A., & McGrath, M. (in press). Pathological altruism—An introduction. In Oakley, B., Knafo, A., Madhavan, G., & Wilson, D. S. (Eds.), Pathological altruism. New York: Oxford University Press.
Plomin, R. (1994). Genetics and experience: The interplay between nature and nurture. Thousand Oaks, CA: Sage.
Plomin, R., DeFries, J. C., & Loehlin, J. C. (1977). Genotype–environment interaction and correlation in the analysis of human behavior. Psychological Bulletin, 85, 309322.
Plomin, R., DeFries, J. C., McClearn, G. E., & McGuffin, P. (2001). Behavioral genetics (4th ed.). New York: Worth.
Price, T. S., Freeman, B., Craig, I. W., Petrill, S. A., Ebersole, L., & Plomin, R. (2000). Infant zygosity can be assigned by parental report questionnaire data. Twin Research, 3, 129133.
Propper, C., & Moore, G. A. (2006). The influence of parenting on infant emotionality: A multi-level psychobiological perspective. Developmental Review, 26, 427460.
Robinson, C. C., Mandleco, B., Olsen, S. F., & Hart, C. H. (1995). Authoritative, authoritarian, and permissive parenting practices: Development of a new measure. Psychological Reports, 77, 819830.
Rubin, K. H., Burgess, K. B., & Hastings, P. D. (2002). Stability and social–behavioral consequences of toddlers' inhibited temperament and parenting behaviors. Child Development, 73, 483495.
Saudino, K. J., Plomin, R., & DeFries, J. C. (1996). Tester-rated temperament at 14, 20, and 24 months: Environmental change and genetic continuity. British Journal of Developmental Psychology, 14, 129144.
Scourfield, J., John, B., Martin, N., & McGuffin, P. (2004). The development of prosocial behaviour in children and adolescents: A twin study. Journal of Child Psychology and Psychiatry, 45, 927935.
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, 10391046.
Staub, E. (1979). Positive social behavior and morality: Socialization and development (Vol. 2). New York: Academic Press.
Turkheimer, E., Haley, A., Waldron, M., D'Onofrio, B., & Gottesman, I. I. (2003). Socioeconomic status modifies heritability of IQ in young children. Psychological Science, 14, 623628.
Van IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2006). DRD47-repeat polymorphism moderates the association between maternal unresolved loss or trauma and infant disorganization. Attachment & Human Development, 8, 291307.
Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Pannebaker, F., & Out, D. (2010). In defence of situational morality: Genetic, dispositional and situational determinants of children's donating to charity. Journal of Moral Education, 39, 120.
Van Lange, P. A. M. (2008). Does empathy trigger only altruistic motivation? How about selflessness or justice? Emotion, 8, 766774.
Volbrecht, M. M., Lemery-Chalfant, K., Aksan, N., Zahn-Waxler, C., & Goldsmith, H. H. (2007). Examining the familial link between positive affect and empathy development in the second year. Journal of Genetic Psychology, 168, 105129.
Whiteside-Mansell, L., Bradley, R., Tresch Owen, M., Randolph, S., & Cauce, A. M. (2003). Parenting and children's behavior at 36 months: Equivalence between African American and European American mother–child dyads. Parenting: Science and Practice, 3, 197234.
Wise, R. A. (2004). Dopamine, learning and motivation. Nature Reviews Neuroscience, 5, 112.
Yarrow, M. R., Zahn-Waxler, C., Barrett, D., Darby J., King, R., Pickett, M., et al. (1976). Dimensions and correlates of prosocial behavior in young children. Child Development, 47, 118125.
Zahn-Waxler, C., Schiro, K., Robinson, J. L., Emde, R. N., & Schmitz, S. (2001). Empathy & prosocial patterns in young MZ and DZ twins: Development and genetic and environmental influences. In Emde, R. N. & Hewitt, J. K. (Eds.), Infancy to early childhood: Genetic and environmental influences on developmental change (pp. 141162). New York: Oxford University Press.
Zahn-Waxler, C., & Van Hulle, C. (in press). Empathy, guilt, and depression: When caring for others becomes costly to children. In Oakley, B., Knafo, A., Madhavan, G., & Wilson, D. S. (Eds.), Pathological altruism. New York: Oxford University Press.
Zarbatany, L., Hartmann, D. P., & Gelfand, D. M. (1985). Why does children's generosity increase with age: Susceptibility to experimenter influence or altruism? Child Development, 56, 746756.


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed