Vantage Sensitivity: Environmental Sensitivity to Positive Experiences as a Function of Genetic Differences
Corresponding Author
Michael Pluess
Queen Mary University of London
Correspondence concerning this article should be addressed to Michael Pluess, Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, United Kingdom. Email: [email protected].Search for more papers by this authorCorresponding Author
Michael Pluess
Queen Mary University of London
Correspondence concerning this article should be addressed to Michael Pluess, Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, United Kingdom. Email: [email protected].Search for more papers by this authorI would like to thank Stephen Manuck for providing the term vantage sensitivity and acknowledge Jay Belsky's contribution to previous coauthored publications on vantage sensitivity, upon which some parts of the current article are based.
Abstract
A large number of gene–environment interaction studies provide evidence that some people are more likely to be negatively affected by adverse experiences as a function of specific genetic variants. However, such “risk” variants are surprisingly frequent in the population. Evolutionary analysis suggests that genetic variants associated with increased risk for maladaptive development under adverse environmental conditions are maintained in the population because they are also associated with advantages in response to different contextual conditions. These advantages may include (a) coexisting genetic resilience pertaining to other adverse influences, (b) a general genetic susceptibility to both low and high environmental quality, and (c) a coexisting propensity to benefit disproportionately from positive and supportive exposures, as reflected in the recent framework of vantage sensitivity. After introducing the basic properties of vantage sensitivity and highlighting conceptual similarities and differences with diathesis-stress and differential susceptibility patterns of gene–environment interaction, selected and recent empirical evidence for the notion of vantage sensitivity as a function of genetic differences is reviewed. The unique contribution that the new perspective of vantage sensitivity may make to our understanding of social inequality will be discussed after suggesting neurocognitive and molecular mechanisms hypothesized to underlie the propensity to benefit disproportionately from benevolent experiences.
References
- Albert, D., Belsky, D. W., Crowley, D. M., Latendresse, S. J., Aliev, F., Riley, B., et al. (2015). Can genetics predict response to complex behavioral interventions? Evidence from a genetic analysis of the Fast Track Randomized Control Trial. Journal of Policy Analysis and Management, 34, 497–518. doi: 10.1002/pam.21811
- Aron, E. N., Aron, A., & Jagiellowicz, J. (2012). Sensory processing sensitivity: A review in the light of the evolution of biological responsivity. Personality and Social Psychology Review, 16, 262–282.
- 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.
- Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to rearing environment depending on dopamine-related genes: New evidence and a meta-analysis. Development and Psychopathology, 23, 39–52.
- Bakker, J., Lieverse, R., Menne-Lothmann, C., Viechtbauer, W., Pishva, E., Kenis, G., et al. (2014). Therapy genetics in mindfulness-based cognitive therapy: Do genes have an impact on therapy-induced change in real-life positive affective experiences?. Translational Psychiatry, 4(4), e384.
- Beach, S. R. H., Brody, G. H., Lei, M. K., Kim, S., Cui, J., & Philibert, R. A. (2014). Is serotonin transporter genotype associated with epigenetic susceptibility or vulnerability? Examination of the impact of socioeconomic status risk on African American youth. Development and Psychopathology, 26, 289–304.
- Beevers, C. G., Marti, C. N., Lee, H. J., Stote, D. L., Ferrell, R. E., Hariri, A. R., et al. (2011). Associations between serotonin transporter gene promoter region (5-HTTLPR) polymorphism and gaze bias for emotional information. Journal of Abnormal Psychology, 120, 187–197.
- Belsky, J. (1997a). Theory testing, effect-size evaluation, and differential susceptibility to rearing influence: The case of mothering and attachment. Child Development, 68, 598–600.
- Belsky, J. (1997b). Variation in susceptibility to rearing influences: An evolutionary argument. Psychological Inquiry, 8, 182–186.
- Belsky, J. (2005). Differential susceptibility to rearing influences: An evolutionary hypothesis and some evidence. In B. Ellis & D. Bjorklund (Eds.), Origins of the social mind: Evolutionary psychology and child development (pp. 139–163). New York: Guilford Press.
- 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, 300–304.
- Belsky, J., Hsieh, K. H., & 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, 301–319.
- Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746–754.
- Belsky, J., & Pluess, M. (2009a). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908.
- Belsky, J., & Pluess, M. (2009b). The nature (and nurture?) of plasticity in early human development. Perspectives on Psychological Science, 4, 345–351.
- Belsky, J., & Pluess, M. (2013). Beyond risk, resilience, and dysregulation: Phenotypic plasticity and human development. Developmental Psychopathology, 25, 1243–1261.
- Boniwell, I., & Ryan, L. (2009). SPARK Resilience: A teacher's guide. London: University of East London.
- Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Developmental Psychopathology, 17, 271–301.
- Brunner, H. G., Nelen, M., Breakefield, X. O., Ropers, H. H., & van Oost, B. A. (1993). Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science, 262(5133), 578–580.
- Bundy, H., Stahl, D., & MacCabe, J. (2011). A systematic review and meta-analysis of the fertility of patients with schizophrenia and their unaffected relatives. Acta Psychiatrica Scandinavica, 123, 98–106.
- 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(5582), 851–854.
- Caspi, A., & Moffitt, T. E. (2006). Gene-environment interactions in psychiatry: Joining forces with neuroscience. Nature Reviews Neuroscience, 7, 583–590.
- Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science, 301(5631), 386–389.
- Chang, F. M., Kidd, J. R., Livak, K. J., Pakstis, A. J., & Kidd, K. K. (1996). The world-wide distribution of allele frequencies at the human dopamine D4 receptor locus. Human Genetics, 98, 91–101.
- Chen, L., Pan, H., Tuan, T. A., Teh, A. L., MacIsaac, J. L., Mah, S. M., et al. (2015). Brain-derived neurotrophic factor (BDNF) Val66Met polymorphism influences the association of the methylome with maternal anxiety and neonatal brain volumes. Dev Psychopathol, 27, 137–150. doi: 10.1017/s0954579414001357
- Chiao, J. Y., & Blizinsky, K. D. (2010). Culture-gene coevolution of individualism-collectivism and the serotonin transporter gene. Proceedings: Biological Sciences, 277(1681), 529–537.
- Cleveland, H. H., Schlomer, G. L., Vandenbergh, D. J., Feinberg, M., Greenberg, M., Spoth, R., et al. (2015). The conditioning of intervention effects on early adolescent alcohol use by maternal involvement and dopamine receptor D4 (DRD4) and serotonin transporter linked polymorphic region (5-HTTLPR) genetic variants. Development and Psychopathology, 27, 51–67.
- Ding, Y., Chi, H., Grady, D. L., Morishima, A., Kidd, J., Kidd, K. K., et al. (2002). Evidence of positive selection acting at the human dopamine DF gene locus. Proceedings of the National Academy of Sciences, 99, 309–314.
- Drury, S. S., Gleason, M. M., Theall, K. P., Smyke, A. T., Nelson, C. A., Fox, N. A., et al. (2012). Genetic sensitivity to the caregiving context: The influence of 5HTTLPR and BDNF Val66Met on indiscriminate social behavior. Physiology and Behavior, 106, 728–735.
- Duncan, L. E., & Keller, M. C. (2011). A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. American Journal of Psychiatry, 168, 1041–1049.
- Eaves, L., Heath, A., Martin, N., Maes, H., Neale, M., Kendler, K., et al. (1999). Comparing the biological and cultural inheritance of personality and social attitudes in the Virginia 30,000 study of twins and their relatives. Twin Research, 2(2), 62–80.
- Eley, T. C., Hudson, J. L., Creswell, C., Tropeano, M., Lester, K. J., Cooper, P., et al. (2012). Therapygenetics: The 5HTTLPR and response to psychological therapy. Molecular Psychiatry, 17, 236–241.
- 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.
- Faraone, S. V., Doyle, A. E., Mick, E., & Biederman, J. (2001). Meta-analysis of the association between the 7-repeat allele of the dopamine D(4) receptor gene and attention deficit hyperactivity disorder. American Journal of Psychiatry, 158, 1052–1057.
- Felmingham, K. L., Dobson-Stone, C., Schofield, P. R., Quirk, G. J., & Bryant, R. A. (2013). The brain-derived neurotrophic factor Val66Met polymorphism predicts response to exposure therapy in posttraumatic stress disorder. Biological Psychiatry, 73, 1059–1063.
- Gottesman, I. I., & Shields, J. (1967). A polygenic theory of schizophrenia. Proceedings of the National Academy of Sciences, 58, 199–205.
- Homberg, J. R., & Lesch, K. P. (2011). Looking on the bright side of serotonin transporter gene variation. Biological Psychiatry, 69, 513–519.
- Huebner, E. S. (1991). Initial development of the Students’ Life Satisfaction Scale. School Psychology International, 12, 231–243.
10.1177/0143034391123010 Google Scholar
- Jang, K. L., Livesley, W. J., & Vernon, P. A. (1996). Heritability of the Big Five personality dimensions and their facets: A twin study. Journal of Personality, 64, 577–591.
- Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011). The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: Evidence of genetic moderation. Archives of General Psychiatry, 68, 444–454.
- Kegel, C. A. T., Bus, A. G., & van Ijzendoorn, M. H. (2011). Differential susceptibility in early literacy instruction through computer games: The role of the dopamine D4 receptor gene (DRD4). Mind, Brain, and Education, 5(2), 71–78.
- 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.
- Kluger, A. N., Siegfried, Z., & Ebstein, R. P. (2002). A meta-analysis of the association between DRD4 polymorphism and novelty seeking. Molecular Psychiatry, 7, 712–717.
- Luijk, M., Tharner, A., Bakermans-Kranenburg, M. J., van Ijzendoorn, M. H., Jaddoe, V. W. V., Hofman, A., et al. (2011). The association between parenting and attachment security is moderated by a polymorphism in the mineralocorticoid receptor gene: Evidence for differential susceptibility. Biological Psychology, 88, 37–40.
- Luzzatto, L. (2012). Sickle cell anaemia and malaria. Mediterranean Journal of Hematology and Infectious Diseases, 4, e2012065. doi:10.4084/mjhid.2012.065
- Mackenbach, J. P., Stirbu, I., Roskam, A. J. R., Schaap, M. M., Menvielle, G., Leinsalu, M., et al. (2008). Socioeconomic inequalities in health in 22 European countries. New England Journal of Medicine, 358, 2468–2481.
- Manuck, S. B. (2011). Delay discounting covaries with childhood socioeconomic status as a function of genetic variation in the dopamine D4 receptor (DRD4). Paper presented at the Society for Research in Child Development, Montreal, Canada.
- Manuck, S. B., & McCaffery, J. M. (2014). Gene-environment interaction. In S. T. Fiske (Ed.), Annual review of psychology (Vol. 65, pp. 41–70). Palo Alto, CA: Annual Reviews.
10.1146/annurev-psych-010213-115100 Google Scholar
- Monroe, S. M., & Simons, A. D. (1991). Diathesis-stress theories in the context of life stress research: Implications for the depressive disorders. Psychological Bulletin, 110, 406–425.
- Munafo, M. R., Brown, S. M., & Hariri, A. R. (2008). Serotonin transporter (5-HTTLPR) genotype and amygdala activation: A meta-analysis. Biological Psychiatry, 63, 852–857.
- Munafo, M. R., Freimer, N. B., Ng, W., Ophoff, R., Veijola, J., Miettunen, J., et al. (2009). 5-HTTLPR genotype and anxiety-related personality traits: A meta-analysis and new data. American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics, 150(2), 271–281.
- Plomin, R., Owen, M. J., & McGuffin, P. (1994). The genetic basis of complex human behaviors. Science, 264(5166), 1733–1739.
- Pluess, M. (2015). Individual differences in environmental sensitivity. Child Development Perspectives, 9, 138–143. doi: 10.1111/cdep.12120
- Pluess, M., & Bartley, M. (2015). Childhood conscientiousness predicts the social gradient of smoking in adulthood: A life course analysis. Journal of Epidemiology and Community Health, 69, 330–338.
- Pluess, M., & Belsky, J. (2013). Vantage sensitivity: Individual differences in response to positive experiences. Psychological Bulletin, 139, 901–916.
- Pluess, M., & Belsky, J. (2015). Vantage sensitivity: Genetic susceptibility to effects of positive experiences. In M. Pluess (Ed.), Genetics of psychological well-being (pp. 193–210). Oxford: Oxford University Press.
10.1093/acprof:oso/9780199686674.003.0012 Google Scholar
- Pluess, M., Boniwell, I., Hefferon, K., & Tunariu, A. (2015). Evaluation of a school-based resilience-promoting intervention in a high-risk population: An exploratory mixed-methods trial.
- Pluess, M., & Meaney, M. J. (2015). Genes, environment, and psychological well-being. In M. Pluess (Ed.), Genetics of psychological well-being (pp. 249–265). Oxford: Oxford University Press.
- Pluess, M., Stevens, S., & Belsky, J. (2013). Differential susceptibility: Developmental and evolutionary mechanisms of gene-environment interactions. In M. Legerstee, D. W. Haley, & M. H. Bornstein (Eds.), The infant mind: Origins of the social brain (pp. 77–96). New York: Guilford Press.
- Power, R. A., Kyaga, S., Uher, R., MacCabe, J. H., Langstrom, N., Landen, M., et al. (2013). Fecundity of patients with schizophrenia, autism, bipolar disorder, depression, anorexia nervosa, or substance abuse vs. their unaffected siblings. JAMA Psychiatry, 70, 22–30.
- Risch, N., Herrell, R., Lehner, T., Liang, K. Y., Eaves, L., Hoh, J., et al. (2009). Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: A meta-analysis. Journal of the American Medical Association, 301, 2462–2471.
- Robbins, T. W., & Everitt, B. J. (1999). Motivation and reward. In M. J. Zigmond, S. C. Bloom, S. C. Landis, J. L. Roberts, & L. R. Squire (Eds.), Fundamental neuroscience (pp. 1245–1260). San Diego, CA: Academic Press.
- Roiser, J. P., Rogers, R. D., Cook, L. J., & Sahakian, B. J. (2006). The effect of polymorphism at the serotonin transporter gene on decision-making, memory and executive function in ecstasy users and controls. Psychopharmacology, 188, 213–227.
- Rutter, M., Moffitt, T. E., & Caspi, A. (2006). Gene-environment interplay and psychopathology: Multiple varieties but real effects. Journal of Child Psychology and Psychiatry, 47, 226–261.
- Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316.
- Sen, S., Burmeister, M., & Ghosh, D. (2004). Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics, 127(1), 85–89.
- Sergerie, K., Chochol, C., & Armony, J. L. (2008). The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 32, 811–830.
- Shanahan, M. J., & Hofer, S. M. (2005). Social context in gene–environment interactions: Retrospect and prospect. Journals of Gerontology, Series B: Psychological Sciences and Social Sciences, 60(Special Issue 1), 65–76.
- Sulik, M. J., Eisenberg, N., Spinrad, T. L., Lemery-Chalfant, K., Swann, G., Silva, K. M., et al. (2014). Interactions among catechol-O-methyltransferase genotype, parenting, and sex predict children's internalizing symptoms and inhibitory control: Evidence for differential susceptibility. Development and Psychopathology, 1–15.
- Sweitzer, M. M., Halder, I., Flory, J. D., Craig, A. E., Gianaros, P. J., Ferrell, R. E., et al. (2012). Polymorphic variation in the dopamine D4 receptor predicts delay discounting as a function of childhood socioeconomic status: Evidence for differential susceptibility. Social Cognitive & Affective Neuroscience. doi: 10.1093/scan/nss020
10.1093/scan/nss020 Google Scholar
- Szyf, M., & Pluess, M. (2015). Epigenetics and well-being: Optimal adaptation to the environment. In M. Pluess (Ed.), Genetics of psychological well-being (pp. 211–230). Oxford: Oxford University Press.
10.1093/acprof:oso/9780199686674.003.0013 Google Scholar
- Taylor, A., & Kim-Cohen, J. (2007). Meta-analysis of gene–environment interactions in developmental psychopathology. Development and Psychopathology, 19, 1029–1037.
- Uher, R. (2009). The role of genetic variation in the causation of mental illness: An evolution-informed framework. Molecular Psychiatry, 14, 1072–1082. doi: 10.1038/mp.2009.85
- Uher, R., & McGuffin, P. (2010). The moderation by the serotonin transporter gene of environmental adversity in the etiology of depression: 2009 update. Molecular Psychiatry, 15, 18–22.
- Vallender, E. J., & Lahn, B. T. (2004). Positive selection on the human genome. Human Molecular Genetics, 13(Spec No 2), R245–254.
- van IJzendoorn, M. H., Belsky, J., & Bakermans-Kranenburg, M. J. (2012). Serotonin transporter genotype 5HTTLPR as a marker of differential susceptibility? A meta-analysis of child and adolescent gene-by-environment studies. Translational Psychiatry, 2, e147. doi: 10.1038/tp.2012.73
- Way, B. M., & Taylor, S. E. (2010). Social influences on health: Is serotonin a critical mediator? Psychosomatic Medicine, 72, 107–112.
- Wilker, S., Pfeiffer, A., Kolassa, S., Elbert, T., Lingenfelder, B., Ovuga, E., et al. (2014). The role of FKBP5 genotype in moderating long-term effectiveness of exposure-based psychotherapy for posttraumatic stress disorder. Translational Psychiatry, 4(6), e403.
- Zeanah, C. H., Nelson, C. A., Fox, N. A., Smyke, A. T., Marshall, P., Parker, S. W., et al. (2003). Designing research to study the effects of institutionalization on brain and behavioral development: The Bucharest Early Intervention Project. Development and Psychopathology, 15, 885–907.
- Zuckerman, M. (1999). Vulnerability to Psychopathology: A Biosocial Model. Washington, DC: American Psychological Association.
10.1037/10316-000 Google Scholar