Heritability in the Era of Molecular Genetics: Some Thoughts for Understanding Genetic Inﬂuences on Behavioural Traits

European Journal of Personality, Eur. J. Pers. 25: 254–266 (2011) Published online (wileyonlinelibrary.com) DOI: 10.1002/per.836 Heritability in the Era of Molecular Genetics: Some Thoughts for Understanding Genetic Influences on Behavioural Traits WENDY JOHNSON1,2*, LARS PENKE1 and FRANK M. SPINATH3 1Centre for Cognitive Ageing and Cognitive Epidemiology and Department of Psychology, University of Edinburgh, Edinburgh, UK 2Department of Psychology, University of Minnesota, Minneapolis, Minnesota, USA 3Department of Psychology, Saarland University, Saarbruecken, Germany Abstract: Genetic influences on behavioural traits are ubiquitous. When behaviourism was the dominant paradigm in psychology, demonstrations of heritability of behavioural and psychological constructs provided important evidence of its limitations. Now that genetic influences on behavioural traits are generally accepted, we need to recognise the limitations of heritability as an indicator of both the aetiology and likelihood of discovering molecular genetic associations with behavioural traits. We review those limitations and conclude that quantitative genetics and genetically informative research designs are still critical to understanding the roles of gene‐environment interplay in developmental processes, though not necessarily in the ways commonly discussed. Copyright © 2011 John Wiley & Sons, Ltd. Key words: genetic influences; twin study; heritability Much is often made of new findings of the presence of environmental influences but emphasised that these genetic influences on measures of behavioural traits or environmental influences are generally nonshared, thus psychological constructs. We live in an age of fascination confounded with measurement error and likely to be much with genetic mechanisms. Psychological and medical smaller than estimated. They even pointed out that some researchers seek the genetic determinants of illnesses and of the legitimately nonshared environmental influences undesirable behaviours, with the aim of eventually develop- could lead to biological determination as well, because of ing appropriate biochemical interventions. Sociologists, ‘prenatal hormonal environment, minor brain damage or historians and even economists seek evolutionary explana- infection, or the imperfect operation of genetic mechanisms’ tions for current social and behavioural patterns, with the (page 176), thus rendering the proportion of personality aim of eventually developing policies that accurately reflect variation potentially subject tomanipulationbythepostnatal human nature. Thus, findings of genetic influences on new environment even smaller. measures of behaviours or psychological constructs are often More recently, in a journal as high profile as the used to justify claims of the validity of the measures, their Proceedings of the National Academy of Sciences USA, bases in biology and, by extension, the reality of the Wallace, Cesarini, Lichtenstein, and Johannesson (2007) constructs, their evolutionary significance, the appropriate- reported that the heritability of responder behaviour in a ness of policies accepting present social circumstances as game‐theoretical experiment was 42% in the Swedish Twin inevitable and the expense of molecular genetic search for Registry. This behaviour was willingness to deviate from the specific genes involved. maximally personally advantageous game strategies in order For example, in developing their Five Factor Theory of to punish opponent behaviour perceived to be unfair. The personality, McCrae et al. (2000) took the strong position authors pointed to the consistency of their findings that this that personality traits are ‘endogenous dispositions, influenced behaviour was heritable with those from other studies of not at all by the environment’ (page 175). Though acknowl- economically relevant social attitudes. They also pointed to edging it to be an oversimplification, they justified this position other researchers’ observations of increased testosterone by pointing to the heritability of personality—not only of levels and activation in the dorsolateral prefrontal cortex factors such as extraversion and neuroticism which are during game performance as evidence of the biological generally recognised to be temperamental but also of the other significance of their findings. They noted that their findings major dimensions in their Five Factor Theory, and even of had important implications for economic theory and policy more specific aspects of personality such as their underlying as well as for understanding behaviour in experimental facets. They noted that the same studies that show that conditions and how observed patterns of game responding personality is heritable also show that it is subject to behaviour may have evolved. Rushton, Bons, and Hur (2008) carried such inferences even further. They demonstrated that they could obtain *Correspondence to: Wendy Johnson, Centre for Cognitive Ageing and Cognitive Epidemiology and Department of Psychology, 7 George Square, general factors of personality in several samples and that Edinburgh, UK EH8 9JZ. E‐mail: [email protected] these general factors of personality showed substantial Received 13 April 2010 Copyright © 2011 John Wiley & Sons, Ltd. Revised 15 December 2010, Accepted 15 December 2010 Understanding heritability 255 heritability. Noting that the genetic influences appeared to be behaviour: the specific situation and the actor’s environ- nonadditive (subject to interactions among gene loci), they mental history for both matter but so does the genotype of concluded that they had obtained evidence for evolutionary the actor. Moreover, outside the lab (and even inside it, as selection effects on the general factor of personality, with participation in psychology experiments is not random in the those higher on this factor likely evidencing higher population), the actor’s genotype is involved in the reproductive fitness. likelihood that any specific situation will even be encoun- There is no doubt about the findings of heritability of tered, let alone how the actor will behave in that situation once behavioural traits, whether they be personality or ability in it is encountered. Anyone could be mugged and responses to specific or in general, or particular patterns of activities such mugging will vary, but people who have a tendency to walk as game response, or TV viewing. In the last 30 years, the field alone at night in dangerous areas are more likely to end up of behaviour genetics has accomplished a paradigm shift in displaying their individual responses to mugging. As psychology, biology and sociology, primarily through the psychologists, we want to understand why people behave as estimation of heritability in trait after trait after trait. It is they do, which means understanding not only the behaviour now generally accepted that behavioural traits are subject to typically displayed but how people come to be in positions in genetic influences and genetic influences on behavioural which the behaviour is relevant. The important question is no traits are ubiquitous, so much so that Turkheimer (2000) longer whether genetic influences are involved in this—by enshrined this as the First Law of Behaviour Genetics. This now, we know that they are—but how they are involved. general prevalence of genetic influences is of critical Ignoring or disregarding genetic influences is impossible if importance for our understanding that major sources of any true understanding is to be achieved. Estimating behavioural differences lie in differences intrinsic to each heritability provides a rough and ready way of cutting the individual, and therefore, it is a great accomplishment of processes involved into genetic and environmental pieces, and behaviour genetics that they are now so firmly established the persistent observation that the genetic piece is not small and widely accepted. But what exactly does it mean for the has real meaning. But heritability alone does not help us underlying biology, what does it have to do with evolution, identify and understand the processes that generate patterns of and what does it tell us about the inevitability of life behaviour nor what can or cannot be done about them. outcomes and social structures if all behavioural traits are moderately heritable? This is a more subtle question. We perceive that fascination with the presence of genetic UNDERSTANDING THE LIMITATIONS OF influences on behavioural traits has outstripped awareness HERITABILITY ESTIMATES of the subtleties involved in heritability statistics among many, and the time has come to revisit such details, The limitations of heritability estimates for understanding particularly in the light of recent developments in molecular underlying biology have long been known to behaviour genetics. That is the purpose of this target article. It is in no geneticists but not necessarily to the many social scientists sense intended to question the validity of heritability statistics who are becoming newly interested in the presence of genetic as indicators of the presence of genetic influences on influences on behavioural traits. Fortunately for psycholo- behavioural and psychological traits but to sharpen the ability gists, many of the limitations of heritability estimates for of psychologists to make effective interpretive use of the understanding biology are related to psychometric principles, information they provide. so the concepts involved should have a familiar ring. Simply put, better measurement in and of itself

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