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Boys' serotonin transporter genotype affects maternal behavior through self-control: A case of evocative gene–environment correlation

Published online by Cambridge University Press:  11 February 2013

Roni Pener-Tessler
Affiliation:
Hebrew University of Jerusalem
Reut Avinun
Affiliation:
Hebrew University of Jerusalem
Florina Uzefovsky
Affiliation:
Hebrew University of Jerusalem
Shany Edelman
Affiliation:
Hebrew University of Jerusalem
Richard P. Ebstein
Affiliation:
National University of Singapore
Ariel Knafo*
Affiliation:
Hebrew University of Jerusalem
*
Address correspondence and reprint requests to: Ariel Knafo, Department of Psychology, Hebrew University of Jerusalem, Mount Scopus, Jerusalem 91905, Israel; E-mail: msarielk@huji.ac.il.

Abstract

Self-control, involving processes such as delaying gratification, concentrating, planning, following instructions, and adapting emotions and behavior to situational requirements and social norms, may have a profound impact on children's adjustment. The importance of self-control suggests that parents are likely to modify their parenting based on children's ability for self-control. We study the effect of children's self-control, a trait partially molded by genetics, on their mothers' parenting, a process of evocative gene–environment correlation. Israeli 3.5-year-old twins (N = 320) participated in a lab session in which their mothers' parenting was observed. DNA was available from most children (N = 228). Mothers described children's self-control in a questionnaire. Boys were lower in self-control and received less positive parenting from their mothers, in comparison with girls. For boys, and not for girls, the serotonin transporter linked polymorphic region gene predicted mothers' levels of positive parenting, an effect mediated by boys' self-control. The implications of this evocative gene–environment correlation and the observed sex differences are discussed.

Type
Special Section Articles
Copyright
Copyright © Cambridge University Press 2013

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References

Anderson, K. E., Lytton, H., & Romney, D. M. (1986). Mothers' interactions with normal and conduct-disordered boys: Who affects whom? Developmental Psychology, 22, 604609.CrossRefGoogle Scholar
Avinun, R., & Knafo, A. (in press). The Longitudinal Israeli Study of Twins (LIST)—An integrative view of social development. Twin Research and Human Genetics.Google Scholar
Beaver, K. M., Ferguson, C. J., & Lynn-Whaley, J. (2010). The association between parenting and levels of self-control: A genetically informative analysis. Criminal Justice and Behavior, 37, 10451065.CrossRefGoogle Scholar
Beaver, K. M., Ratchford, M., & Ferguson, C. J. (2009). Evidence of genetic and environmental effects on the development of low self-control. Criminal Justice and Behavior, 36, 11581172.CrossRefGoogle Scholar
Beaver, K. M., Wright, J. P., DeLisi, M., & Vaughn, M. G. (2008). Genetic influences on the stability of low self-control: Results from a longitudinal sample of twins. Journal of Criminal Justice, 36, 478485.CrossRefGoogle Scholar
Belsky, J., & Beaver, K. M. (2011). Cumulative-genetic plasticity, parenting and adolescent self-regulation. Journal of Child Psychology and Psychiatry, 52, 619626.CrossRefGoogle ScholarPubMed
Berger, A. (2011). Self-regulation: Brain, cognition, and development. Washington, DC: American Psychological Association.CrossRefGoogle Scholar
Bierman, K. L., Nix, R. L., Greenberg, M. T., Blair, C., & Domitrovich, C. E. (2008). Executive functions and school readiness intervention: Impact, moderation, and mediation in the Head Start REDI program. Developmental Psychopathology, 20, 821843.CrossRefGoogle ScholarPubMed
Block, J., & Block, J. H. (2006). Venturing a 30-year longitudinal study. American Psychologist, 61, 315327.CrossRefGoogle ScholarPubMed
Breton, J. J., Bergeron, L., Valla, J. P., Berthiaume, C., Gaudet, N., Lambert, J., et al. (1999). Quebec Child Mental Health Survey: Prevalence of DSM-III-R mental health disorders. Journal of Child Psychology and Psychiatry and Allied Disciplines, 40, 375384.CrossRefGoogle ScholarPubMed
Calati, R., De Ronchi, D., Bellini, M., & Serretti, A. (2011). The 5-HTTLPR polymorphism and eating disorders: A meta-analysis. International Journal of Eating Disorders, 44, 191199.CrossRefGoogle ScholarPubMed
Canli, T., & Lesch, K. P. (2007). Long story short: The serotonin transporter in emotion regulation and social cognition. Nature Neuroscience, 10, 11031109.CrossRefGoogle ScholarPubMed
Carlo, G., Raffaelli, M., Laible, D. J., & Meyer, K. A. (1999). Why are girls less physically aggressive than boys? Personality and parenting mediators of physical aggression. Sex Roles, 40, 711729.CrossRefGoogle Scholar
Carter, A. S., Briggs-Gowan, M. G., Jones, S. M., & Little, T. D. (2003). The Infant–Toddler Social and Emotional Assessment (ITSEA): Factor structure, reliability, and validity. Journal of Abnormal Child Psychology, 31, 495514.CrossRefGoogle ScholarPubMed
Carver, C. S., Johnson, S. L., Joormann, J., Kim, Y., & Nam, J. Y. (2011). Serotonin transporter polymorphism interacts with childhood adversity to predict aspects of impulsivity. Psychological Science, 22, 589.CrossRefGoogle ScholarPubMed
Caspi, A., & Silva, P. A. (1995). Temperamental qualities at age three predict personality traits in young adulthood: Longitudinal evidence from a birth cohort. Child Development, 66, 486498.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 Part B: Neuropsychiatric Genetics, 147, 2732.CrossRefGoogle Scholar
DeLisi, M., Beaver, K. M., Vaughn, M. G., Trulson, C. R., Kosloski, A. E., Drury, A. J., et al. (2010). Personality, gender, and self-control theory revisited: Results from a sample of institutionalized juvenile delinquents. Applied Psychology in Criminal Justice, 6, 3146.Google Scholar
Dix, T. (1991). The affective organization of parenting: Adaptive and maladaptive processes. Psychological Bulletin, 110, 325.CrossRefGoogle ScholarPubMed
Duckworth, A. L., & Seligman, M. E. P. (2005). Self-discipline outdoes IQ in predicting academic performance of adolescents. Psychological Science, 16, 939944.CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R.A., Bemzweig, J., Karbon, M., Poulin, R., & Hanis, L. (1993). The relations of emotionality and regulation to preschoolers' social skills and sociometric status. Child Development, 64, 14181438.CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R. A., Guthrie, I. K., & Reise, M. (2000). Dispositional emotionality and regulation: Their role in predicting quality of social functioning. Journal of Personality and Social Psychology, 78, 136157.CrossRefGoogle ScholarPubMed
Eisenberg, N., Smith, C. L., Sadovsky, A., & Spinrad, T. L. (2004). Effortful control: Relations with emotion regulation, adjustment, and socialization in childhood. In Baumeister, R. F. & Vohs, K. (Eds.), Handbook of self-regulation: Research, theory and applications (pp. 259282). New York: Guilford Press.Google Scholar
Fink, G., Sumner, B., Rosie, R., Wilson, H., & McQueen, J. (1999). Androgen actions on central serotonin neurotransmission: Relevance for mood, mental state and memory. Behavioural Brain Research, 105, 5368.CrossRefGoogle ScholarPubMed
Fortuna, K., van IJzendoorn, M. H., Mankuta, D., Kaitz, M., Avinun, R., Ebstein, R. P., et al. (2011). Differential genetic susceptibility to child risk at birth in predicting observed maternal behavior. PLoS ONE, 6, 18.CrossRefGoogle ScholarPubMed
Frost, R. O., Steketee, G., Cohn, L., & Griess, K. (1994). Personality traits in subclinical and non-obsessive-compulsive volunteers and their parents. Behaviour Research and Therapy, 32, 4756.CrossRefGoogle ScholarPubMed
Gershoff, E. T. (2002). Corporal punishment by parents and associated child behaviors and experiences: A meta-analytic and theoretical review. Psychological Bulletin, 128, 539579.CrossRefGoogle ScholarPubMed
Goldsmith, H. H. (1991). A zygosity questionnaire for young twins: A research note. Behavior Genetics, 21, 257269.CrossRefGoogle ScholarPubMed
Goldsmith, H. H., Buss, K. A., & Lemery, K. S. (1997). Toddler and childhood temperament: Expanded content, stronger genetic evidence, new evidence for the importance of environment. Developmental Psychology, 33, 891905.CrossRefGoogle ScholarPubMed
Goodman, R. (1997). The Strengths and Difficulties Questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38, 581586.CrossRefGoogle ScholarPubMed
Grusec, J. E., & Goodnow, J. J. (1994). Impact of parental discipline methods on the child's internalization of values: A reconceptualization of current points of view. Developmental Psychology, 30, 419.CrossRefGoogle Scholar
Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297, 400.CrossRefGoogle ScholarPubMed
Hayden, E. P., Klein, D. N., Dougherty, L. R., Olino, T. M., Laptook, R. S., Dyson, M. W., et al. (2010). The dopamine D2 receptor and depressive and anxious symptoms in childhood: Associations and evidence for gene–environment correlation and gene–environment interaction. Psychiatric Genetics, 20, 304310.CrossRefGoogle ScholarPubMed
Houts, R. M., Caspi, A., Pianta, R. C., Arseneault, L., & Moffitt, T. E. (2010). The challenging pupil in the classroom: The effect of the child on the teacher. Psychological Science. Advance online publication. doi:10.1177/095679761038804CrossRefGoogle ScholarPubMed
Hughes, J. R., & Gottlieb, L. N. (2002). The effects of the Webster–Stratton parenting program on maltreating families: Fostering strengths. Child Abuse and Neglect, 28, 10811097.CrossRefGoogle Scholar
Jaffee, S. R., Caspi, A., Moffitt, T. E., Polo-Tomas, M., Price, T. S., & Taylor, A. (2004). The limits of child effects: Evidence for genetically mediated child effects on corporal punishment but not on physical maltreatment. Developmental Psychology, 40, 10471057.CrossRefGoogle Scholar
Jenkins, J. M., Rasbash, J. R., & O'Connor, T. G. (2003). The role of the shared family context in differential parenting. Developmental Psychology, 39, 99113.CrossRefGoogle ScholarPubMed
Jovanovic, H., Lundberg, J., Karlsson, P., Cerin, Å., Saijo, T., Varrone, A., et al. (2008). Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. NeuroImage, 39, 14081419.CrossRefGoogle ScholarPubMed
Karreman, A., van Tuijl, C., van Aken, M. A. G., & Dekovic, M. (2006). Parenting and self-regulation in preschoolers: A meta-analysis. Infant and Child Development, 15, 561579.CrossRefGoogle Scholar
Kaye, W., Gendall, K., & Strobe, M. (1998). Serotonin neuronal function and selective serotonin reuptake inhibitor treatment in anorexia and bulimia nervosa. Biological Psychiatry, 44, 825838.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Knafo, A., & Galansky, N. (2008). The influence of children on their parents' values: An under-researched topic. Social and Personality Psychology Compass, 2, 11431161.CrossRefGoogle Scholar
Kochanska, G. (1995). Children's temperament, mothers' discipline, and security of attachment: Multiple pathways to emerging internalization. Child Development, 66, 597615.CrossRefGoogle Scholar
Kochanska, G. (1997). Mutually responsive orientation between mothers and their young children: Implications for early socialization. Child Development, 68, 94112.CrossRefGoogle ScholarPubMed
Kochanska, G., & Aksan, N. (1995). Mother–child mutually positive affect, the quality of child compliance to requests and prohibitions, and maternal control as correlates of early internalization. Child Development, 66, 236254.CrossRefGoogle Scholar
Kochanska, G., & Knaack, A. (2003). Effortful control as a personality characteristic of young children: Antecedents, correlates, and consequences. Journal of Personality, 71, 10871112.CrossRefGoogle ScholarPubMed
Kochanska, G., Philibert, R. A., & Barry, R. A. (2009). Interplay of genes and early mother–child relationship in the development of self-regulation from toddler to preschool age. Journal of Child Psychology and Psychiatry, 50, 13311338.CrossRefGoogle ScholarPubMed
Kremen, A. M., & Block, J. (1998). The roots of ego-control in young adulthood: Links with parenting in early childhood. Journal of Personality and Social Psychology, 75, 10621075.CrossRefGoogle ScholarPubMed
Kuczynski, L., Marshall, S., & Schell, K. (1997). Value socialization in a bidirectional context. In Grusec, J. E. & Kuczynski, L. (Eds.), Parenting and the internalization of values: A handbook of contemporary theory (pp. 2350). New York: Wiley.Google Scholar
Kuhnen, C. M., & Chiao, J. Y. (2009). Genetic determinants of financial risk taking. PLoS ONE, 4, e4362.CrossRefGoogle ScholarPubMed
LaGrange, T. C., & Silverman, R. A. (1999). Low self-control and opportunity: Testing the general theory of crime as an explanation for gender differences in delinquency. Criminology, 37, 4172.CrossRefGoogle Scholar
Lee, J. H., Kim, H. T., & Hyun, D. S. (2003). Possible association between serotonin transporter promoter region polymorphism and impulsivity in Koreans. Psychiatry Research, 118, 1924.CrossRefGoogle ScholarPubMed
Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274, 15271531.CrossRefGoogle ScholarPubMed
Letzring, T. D., Block, J., & Funder, D. C. (2005). Ego-control and ego-resiliency: Generalization of self-report scales based on personality descriptions from acquaintances, clinicians, and the self. Journal of Research in Personality, 39, 395422.CrossRefGoogle Scholar
Li, D., Sham, P. C., Owen, M. J., & He, L. (2006). Meta-analysis shows significant association between dopamine system genes and attention deficit hyperactivity disorder (ADHD). Human Molecular Genetics, 15, 22762284.CrossRefGoogle ScholarPubMed
Li, J., Wang, Y., Zhou, R., Zhang, H., Yang, L., Wang, B., et al. (2007). Association between polymorphisms in serotonin transporter gene and attention deficit hyperactivity disorder in Chinese Han subjects. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 144, 1419.CrossRefGoogle Scholar
Lucht, M., Barnow, S., Schroeder, W., Grabe, H., Finckh, U., John, U., et al. (2006). Negative perceived paternal parenting is associated with dopamine D2 receptor exon 8 and GABA(A) Alpha 6 receptor variants. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 141, 167172.CrossRefGoogle Scholar
Lytton, H., & Romney, D. M. (1991). Parents' differential socialization of boys and girls: A meta-analysis. Psychological Bulletin, 109, 267296.CrossRefGoogle Scholar
Manor, I., Eisenberg, J., Tyano, S., Sever, Y., Cohen, H., Ebstein, R. P., et al. (2001). Family-based association study of the serotonin transporter promoter region polymorphism (5-HTTLPR) in attention deficit hyperactivity disorder. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 105, 9195.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Manuck, S. B., Flory, J. D., Ferrell, R. E., Dent, K. M., Mann, J. J., & Muldoon, M. F. (1999). Aggression and anger-related traits associated with a polymorphism of the tryptophan hydroxylase gene. Biological Psychiatry, 45, 603614.CrossRefGoogle ScholarPubMed
McQueen, J. K., Wilson, H., & Fink, G. (1997). Estradiol-17β increase serotonin transporter (SERT) mRNA levels and the density of SERT-binding sites in female rat brain. Molecular Brain Research, 45, 1323.CrossRefGoogle ScholarPubMed
McQueen, J. K., Wilson, H., Sumner, B. E. H., & Fink, G. (1999). Serotonin transporter (SERT) mRNA and binding site densities in male rat brain affected by sex steroid. Molecular Brain Research, 63, 241247.CrossRefGoogle Scholar
Mills-Koonce, W. R., Propper, C. B., Gariepy, J. L., Blair, C., Garrett-Peters, P., & Cox, M. J. (2007). Bidirectional genetic and environmental influences on mother and child behavior: The family system as the unit of analyses. Development and Psychopathology, 19, 10731087.CrossRefGoogle Scholar
Mischel, W., Shoda, Y., & Peake, P. K. (1988). The nature of adolescent competencies predicted by preschool delay of gratification. Journal of Personality and Social Psychology, 54, 687696.CrossRefGoogle ScholarPubMed
Moffitt, T. E., Arseneault, L., Belsky, D., Dickson, N., Hancox, R. J., Harrington, H. L., et al. (2010). A gradient of childhood self-control predicts health, wealth, and public safety. Proceedings of the National Academy of Sciences, 108, 26932698.CrossRefGoogle Scholar
Munafò, M. R., Clark, T. G., Roberts, K. H., & Johnston, E. C. (2006). Neuroticism mediates the association of the serotonin transporter gene with lifetime major depression. Neuropsychobiology, 53, 18.CrossRefGoogle ScholarPubMed
Muthén, L. K., & Muthén, B. O. (1998–2010). Mplus user's guide (6th ed.). Los Angeles: Author.Google Scholar
Nachmias, M., Gunnar, M., Mangelsdorf, S., Parritz, R. H., & Buss, K. (1996). Behavioral inhibition and stress reactivity: The moderating role of attachment security. Child Development, 67, 508522.CrossRefGoogle ScholarPubMed
Nisbett, R. E., Aronson, J., Blair, C., Dickens, W., Flynn, J., Halpern, D. F., et al. (2012). Intelligence: New findings and theoretical developments. American Psychologist. Advance online publication. doi:10.1037/a0026699Google ScholarPubMed
Novak, S. P., & Clayton, R. R. (2001). The influence of school environment and self-regulation on transitions between stages of cigarette smoking: A multilevel analysis. Health Psychology, 20, 196207.CrossRefGoogle ScholarPubMed
Oades, R. D. (2010). The role of serotonin in ADHD. In Müller, C. P & Jacobs, B. L. (Eds.), Handbook of behavioral neuroscience: Vol. 21. Handbook of the behavioral neurobiology of serotonin (pp. 565584). San Diego, CA: Elsevier.CrossRefGoogle Scholar
Pergamin-Hight, L., Bakersmans-Kranenburg, M. J., van IJzendoorn, M. H., & Bar-Haim, Y. (2012). Variations in the promoter region of the serotonin transporter gene and biased attention for emotional information: A meta-analysis. Biological Psychiatry, 71, 373379.CrossRefGoogle ScholarPubMed
Plomin, R., DeFries, J. C., & Loehlin, J. C. (1977). Genotype–environment interaction and correlation in the analysis of human behavior. Psychological Bulletin, 84, 309322.CrossRefGoogle ScholarPubMed
Pratt, T. C., & Cullen, F. T. (2000). The empirical status of Gottfredson and Hirschi's general theory of crime: A meta-analysis. Criminology, 38, 931964.CrossRefGoogle Scholar
Pulkkinen, L., Kokko, K., & Rantanen, J. (2012). Paths from socioemotional behavior in middle childhood to personality in middle adulthood. Developmental Psychology. Advance online publication. doi:10.1037/a0027463CrossRefGoogle ScholarPubMed
Rietveld, M. J. H., Hudziak, J. J., Bartels, M., van Beijsterveldt, C. E. M., & Boomsma, D. I. (2004). Heritability of attention problems in children: Longitudinal results from a study of twins, age 3 to 12. Journal of Child Psychology and Psychiatry, 45, 577588.CrossRefGoogle ScholarPubMed
Rothbart, M. K., Ellis, L. K., & Posner, M. I. (2004). Temperament and self-regulation. In Baumeister, R. F. & Vohs, K. (Eds.), Handbook of self-regulation: Research, theory and applications (pp. 357370). New York: Guilford Press.Google Scholar
Rutter, M., Caspi, A., & Moffitt, T. E. (2003). Using sex differences in psychopathology to study causal mechanisms: Unifying issues and research strategies. Journal of Child Psychology and Psychiatry, 44, 10921115.CrossRefGoogle ScholarPubMed
Samochowiec, J., Syrek, S., Michał, P., Ryzewska-Wódecka, A., Samochowiec, A., Horodnicki, J., et al. (2004). Polymorphisms in the serotonin transporter and monoamine oxidase A genes and their relationship to personality traits measured by the Temperament and Character Inventory and NEO Five-Factor Inventory in healthy volunteers. Neuropsychobiology, 50, 174181.CrossRefGoogle ScholarPubMed
Serretti, A., Mandelli, L., Lorenzi, C., Landoni, S., Calati, R., Insacco, C., et al. (2006). Temperament and character in mood disorders: Influence of DRD4, SERTPR, TPH and MAO-A polymorphisms. Neuropsychobiology, 53, 916.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.CrossRefGoogle ScholarPubMed
Solomon, M. B., & Herman, J. P. (2009). Sex differences in psychopathology: Of gonads, adrenals and mental illness. Physiology & Behavior, 97, 250258.CrossRefGoogle ScholarPubMed
Stoltenberg, S. F., & Vandever, J. M. (2009). Gender moderates the association between 5-HTTLPR and decision-making under ambiguity but not under risk. Neuropharmacology, 58, 423428.CrossRefGoogle Scholar
Tangney, J. P., Baumeister, R. F., & Boone, A. L. (2004). High self-control predicts good adjustment, less pathology, better grades, and interpersonal success. Journal of Personality, 72, 271324.CrossRefGoogle ScholarPubMed
Verona, E., Joiner, T. E., Johnson, F., & Bender, T. W. (2006). Gender specific gene–environment interactions on laboratory-assessed aggression. Biological Psychology, 71, 3341.CrossRefGoogle ScholarPubMed
Williams, R. B., Marchuk, D. A., Gadde, K. M., Barefoot, J. C., Grichnik, K., Helms, M. J., et al. (2003). Serotonin-related gene polymorphisms and central nervous system serotonin function. Neuropsychopharmacology, 28, 533541.CrossRefGoogle ScholarPubMed
Wüst, S., Kumsta, R., Treutlein, J., Frank, J., Entringer, S., Schulze, T. G., et al. (2009). Sex-specific association between the 5-HTT gene-linked polymorphic region and basal cortisol secretion. Psychoneuroendocrinology, 34, 972998.CrossRefGoogle ScholarPubMed
Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008). Disorders of childhood and adolescence: Gender and psychopathology. Annual Review of Clinical Psychology, 4, 275303.CrossRefGoogle ScholarPubMed