Discussion on ‘Heritability in the Era of Molecular Genetics: Some Thoughts for Understanding Genetic Influences on Behavioural Traits’ Wendy Johnson, Lars Penke, and Frank M. Spinath

Abstract

The target paper of Johnson, Penke, and Spinath (2011) provides a broad up‐to‐date summary of the many reasons that limit the usefulness of the concept of heritability for understanding genetic contributions to personality differences. My comment focuses on one main reason why heritability is relatively silent about the roles of specific genes in creating personality differences: heritability refers to the outcome of personality development, not to its molecular basis, and therefore, the effects of nonshared genes can be transformed over development into effects that appear genetic in heritability estimates, and the shared genes can, over development, produce effects that appear to be nonshared environmental. Just as (non)shared environmental effects tell us little about (non)shared environments, (non)shared genetic effects tell us little about (non)shared genes. Copyright © 2011 John Wiley & Sons, Ltd. In the context of personality research, heritability refers to the proportion of observed variance in a personality trait in a particular population that is attributed to trait‐relevant genetic differences in this population. Because the attribution to genetic differences is based on assumptions about the genetic relatedness of relatives (MZ versus DZ twins, biological versus adopted siblings, etc.) that are ultimately based on the probability of sharing genes at the molecular‐genetic level (more precisely: sharing alleles of genes), the concept of heritability seems to refer directly to the molecular‐genetic level. However, heritability is estimated on the basis of the phenotypic similarity of relatives and the extent to which they share genes overall. It thus refers to the similarity of trait‐ relevant overall gene expression, not to the similarity of particular trait‐relevant specific genes. Inferences from the similarity in trait‐relevant gene expression to the similarity in trait‐relevant specific genes rest on the assumption of a 1–1 correspondence between genes and effects of these genes. Such a 1–1 correspondence is a tacit assumption underlying the reasoning of many geneticists and psychologists concerned with genetically informed explanations of personality differences. For example, this tacit assumption drives gene association studies, both single allele and genome‐wide; that is, the search for gene loci at which particular alleles are correlated with trait scores (trait‐relevant genes). More specifically, it is assumed that for a trait with high heritability such as height, it is easier to find genes involved in the trait than for a trait with lower heritability (e.g. neuroticism), and the correlations are expected to be higher. The failure to account for more than 5% of trait heritability by effects of specific genes even in large genome‐wide association studies for very accurately measurable traits such as height led to the announcement of a ‘missing heritability problem’ (Maher, 2008), a bad choice of label because what is missing is not heritability—missing are trait‐relevant alleles. My argument here is that expectations to find trait‐ relevant alleles based on high heritability are misguided because the contribution of each gene to the trait may be too small to be detectable with reasonable sample sizes (one of the standard arguments for explaining ‘the missing heritability’) and because they rest on the assumption of 1–1 correspondences between genes and genetic effects, and this assumption is faulty. Figure 1 illustrates the lack of correspondence between the molecular‐genetic level of genes and the quantitative‐genetic level of genetic effects. Assume that the two genomes G1 and G2 share particular alleles because they are genetically related and do not share other alleles because they are not MZ twins. A 1–1 correspondence view assumes that for any trait, the similarity of the trait‐relevant genetic effects P1 and P2 is due only to the similarities between G1 and G2 (the solid lines in Figure 1). However, there may be cross‐effects indicated by the dotted lines in Figure 1 such that alleles of G1 European Journal of Personality, Eur. J. Pers. 25: 267–286 (2011) Published online (wileyonlinelibrary.com) DOI: 10.1002/per.834