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Epigenetics and the Biological Definition of Gene × Environment Child Development, January/February 2010, Volume 81, Number 1, Pages 41–79 Epigenetics and the Biological Definition of Gene · Environment Interactions Michael J. Meaney McGill University Variations in phenotype reflect the influence of environmental conditions during development on cellular functions, including that of the genome. The recent integration of epigenetics into developmental psychobiol- ogy illustrates the processes by which environmental conditions in early life structurally alter DNA, provid- ing a physical basis for the influence of the perinatal environmental signals on phenotype over the life of the individual. This review focuses on the enduring effects of naturally occurring variations in maternal care on gene expression and phenotype to provide an example of environmentally driven plasticity at the level of the DNA, revealing the interdependence of gene and environmental in the regulation of phenotype. The nature–nurture debate is essentially a question prevention and intervention programs. In the social of the determinants of individual differences in the sciences, and particularly psychology, there has expression of specific traits among members of the generally been an understandable bias in favor of same species. The origin of the terms nature and explanations derived from the ‘‘nurture’’ perspec- nurture has been credited to Richard Mulcaster, a tive, which emphasizes the capacity for environ- British teacher who imagined these influences as mentally induced plasticity in brain structure and collaborative forces that shape child development function. Nevertheless, over recent decades there (West & King, 1987). History has conspired to per- has been a gradual, if at times reluctant acceptance vert Mulcaster’s intent, casting genetic and environ- that genomic variations contribute to individual dif- mental influences as independent agents in the ferences in brain development and function. And field of development. The intent of this article is to thus the integration of genetics into psychology and examine the biological context in which genetic and psychiatry has become one of the more active environmental signals actually operate. The result research areas in the study of neural function. Now of this analysis produces an impression that lies that we have come to accept the idea that genomic close to Mulcaster’s formulation. variation influences brain development and func- Any successful attempt to constructively leverage tion in humans, it is time to consider what this the remarkable advances of the genomic era will should mean in the reformulation of intervention depend upon our ability to understand genetic programs that target children and their families. influences and their interactions with the environ- The idea that variation in the expression of neu- mental context within which they operate. Hinder- ral functions would lie outside the dominion of ing such efforts is the rather arcane notion that we genomic influences is biologically untenable. Like can partition the causes of individual differences any tissue, the development of the mammalian into distinct genetic or environmental spheres of brain and its function occurs as a result of coordi- influence. This issue is of particular importance in nated influences that include heritable variation in the area of child development where research that genomic sequence. What remains as a major chal- examines the origins of individual differences in lenge for the psychological sciences is the develop- complex traits often forms the basis for extensive ment of a conceptual framework from which to intervention or prevention programs (Fisher, Gun- meaningfully understand the results of studies that nar, Chamberlain, & Reid, 2000; Olds et al., 1998). examine brain development and function at the Our assumptions concerning the processes of child level of the genotype. However, we remain mired development influence the design of such pro- in additive models of explanation within which grams. Thus, one of the great challenges at this time phenotypic development rolls out as the cumula- is that of integrating genomics into the design of tive by product of genetic + environmental Correspondence concerning this article should be addressed to Michael J. Meaney, Douglas Mental Health University Institute, Ó 2010, Copyright the Author(s) McGill University, 6875 LaSalle Blvd, Montreal, QC, Canada H4H Journal Compilation Ó 2010, Society for Research in Child Development, Inc. 1R3. Electronic mail may be sent to [email protected]. All rights reserved. 0009-3920/2010/8101-0005 42 Meaney influences, with each discipline adding indepen- ences in neural function (Griffiths & Stotz, 2007; dently to the equation. Science in the postgenomic Griffiths & Tabery, 2008; Moss, 2005). era requires a more sophisticated, biologically The issue becomes even more complicated when informed understanding of the interplay between considering the interaction between gene and envi- gene and environment in defining individual ronment, since the statistical approaches to the differences at the level of complex traits. study of Gene · Environment interactions are com- The fundamental question is that of the relation plicated and not yet fully developed. Indeed, since between genotype and phenotype: How do varia- the time of Fisher and Haldane there has been tions in the genotype influence selected traits at any debate concerning the adequacy of analysis of vari- point over the lifespan? This question is addressed ance (ANOVA) models in detecting Gene · Envi- very differently in epidemiology and the social sci- ronment interactions (Wahlsten, 1990; see also ences than it is in the biological sciences. Indeed, the Griffiths & Stotz, 2007; Griffiths & Tabery, 2008, for actual meaning and interpretation of the term gene historical reviews). The primary objective of this can differ across research domains (Griffiths & Ta- article is to examine the Gene · Environment inter- bery, 2008). For epidemiologists or those employing action from the biological perspective. For whatever epidemiological approaches, genotype–phenotype the difficulties in statistically defining Gene · Envi- relations are defined by statistical probabilities. A ronment interactions, research in biology reveals gene for aggression is thus defined as a genomic that the genome cannot possibly operate indepen- region within which a defined variation in sequence dent of its environmental context. The biological predicts a specific phenotypic outcome, in this case perspective reveals the futility of the nature– one associated with aggressive thoughts or actions. nurture debate and of additive models of genetic Here, genotype–phenotype relations are statistical. and environmental influences in defining pheno- For the biological scientist, genotype–phenotype type. Moreover, recent studies from the field of relations are defined by the actual physical operation epigenetics provide insight into biological mecha- of a genomic region in relation to the proximal cellu- nisms whereby Gene · Environment interactions lar events that directly mediate the behavioral varia- can biochemically alter the genome and thus stably tion as well as the more distal influences that influence individual differences in neural function. regulate the relevant cellular signals. Thus, a gene for Developmentalists studying the enduring effects of aggression would be defined as a genomic region early experience on brain development and func- from which a transcribed product actively partici- tion have long anticipated such processes (Bateson pates in a biological pathway that directly mediates et al., 2004; Gottlieb, 1997, 1998; Schneirla, 1966). the expression of aggressive behaviors. The studies This approach envisions development as an active of Young and colleagues (Donaldson & Young, 2008; process of adaptation that occurs as a function of Hammock & Young, 2005) on the sequence variation the continuous dialog between the genome and its in the vasopressin 1A receptor gene provide an environment. With the integration of epigenetics excellent example. Among voles, subspecies differ- into developmental psychobiology, we can now ences in social behaviors are associated with a begin to define the physical basis for this interactive sequence variation in the vasopressin 1A receptor process. gene and differential expression of the vasopressin 1A receptor. Reversing the pattern of vasopressin 1A receptor expression eliminates the differences in Statistical Approaches to the Study of the selected, vasopressin-mediated social behaviors (see ‘‘Instrumental’’ Gene Robinson, Fernald, & Clayton, 2008, for additional examples). These studies describe a causal geno- Research examining the potential influence of heri- type–phenotype relation. Within the biological sci- table variations in DNA sequences on brain devel- ences, the mere statistical relation between a opment and function in humans has relied largely genomic variation and phenotypic outcome would upon two approaches. The first is a classical epide- not be considered as sufficient basis for the establish- miological approach that involves association or ment of a functional link between the gene (or its linkage analyses that essentially use correlational product) and the relevant variation in phenotype. approaches to describe genotype–phenotype rela- Such differences in perspective have led to rather tions. Much as epidemiological research statistically lively debates between, for example, researchers in associates specific exposures with
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