The concept of heritability in its broadest sense attempts to explain the phenotypical similarities between generations. This refers to the physical constitutions of an organism over time as well to its behaviours. Heritability is based on the question of what are causal factors for the phenotype of a living organism, which happens to resemble that of a parent and kin (Jacquard Reference Jacquard1983; Rose Reference Rose2006). It is believed that because phenotypes cannot be passed on, these similarities are explained best by genetic factors. Genes are copied, and in that way, at least parts of their information is passed on to the next generation (Visscher et al. Reference Visscher, Hill and Wray2008). This constitutes a somewhat exclusive view of genetic heritability. However, it should be noted that independent from genes, behaviours can be copied as well, and large parts of an environment may remain the same between generations.

Behavioural genetics set out to explain how genes may transmit the observed similarities in adaptive and pathological behaviours from one generation to the next (Plomin et al. Reference Plomin, DeFries, McClearn and McGuffin2007). This approach, however, is not only based on a genetic definition of heritability, but also on several assumptions which make the DNA of an organisms its relatively solid and stable base throughout life in an ever-changing environment. Charney has now shown that this base is a much less stable and less homogeneous source for a behavioural phenotype as previously thought. In that, it may also serve less well as the unique source for behavioural similarities between parents and offspring. Here we argue that other heritable factors, which are normally the subject of behavioral neuroscience and social learning research, should also be considered more in depth than they were in behavioural neuroscience and social learning research. This may involve that the definition of heritability needs to be expanded and refined to include also non-genetic factors contributing considerably to the similarities in behaviour within pedigrees and social groups.

To explain similarities between generations, behavioural genetics asked for the establishment of clear relationships between genetic (and epigenetic) variations of the DNA and behavioural traits (Plomin et al. Reference Plomin, DeFries, McClearn and McGuffin2007). While this worked out for some physiological measures, complex behavioural traits resisted a simple reduction to properties of the DNA (Maher Reference Maher2008). In 2003, Caspi et al. introduced a new level of understanding when showing that a genotype (G) may result in a particular phenotype only by an interaction with the environment (E). Henceforth, a great number of studies emerged focusing on the G × E interaction. This was assuming a rather constant genotype at longitudinal (i.e., throughout lifetime) and transversal dimensions (i.e., in all cells of the organism, or at least between blood and brain). However, when considering the G×E interaction, major parts of behavioural trait variance resisted explanation (Maher Reference Maher2008). One reason may be that all three components had been looked at too simplistically. In his article, Charney summarizes the evidence that suggests a major break-up in genetic dogmas. Accordingly, the genetic contribution to heritability of behaviour seems much more complex than previously thought.

It has long been known that genes constitute only a certain degree of the behavioural phenotype (Plomin Reference Plomin1990). This leaves considerable space for the “environment.” Here we suggest that, in parallel to the diversification of genetic factors, environmental influences should be reconsidered. We propose to consider two major categories of E: (a) the passively incurred environmental influences (E _pass) and (b) the actively copied information and behaviour (E _act). E _act may be not only the origin for the transmission of particular behaviours and behavioural disorders (Müller & Schumann Reference Müller and Schumann2011), but also the proximal cause for social interactions and culture (Danchin et al. Reference Danchin, Giraldeau, Valone and Wagner2004). While the ability to copy behaviour from conspecific models is genetically determined, its content (i.e., what kind of behaviours and information are copied) is most likely not (Pagel Reference Pagel2012).

Both environmental components have shared and non-shared components. Shared E _pass would, for example, be the experience of a natural disaster that hits great parts of a population. Non-shared E _pass would be, for example, domestic violence as experienced by a single child. The shared part of E _act can be considered as “public information” – knowledge every member of a group has access to (Boyd et al. Reference Boyd, Richerson and Henrich2011; Danchin et al. Reference Danchin, Giraldeau, Valone and Wagner2004). Shared E _act may also comprise “cognitive behaviours” such as verbally transmitted strategies of reasoning that form a “cognitive phenotype” (Pinker Reference Pinker2010). The non-shared E _act may comprise those socially learned behaviours and information that are restricted to an individual; that is, the source is not accessible in the same way for other individuals.

The conceptual differentiation of the E factor in E _pass and E _act allows for a discussion of non-genetic heritability of behaviour. The potential advantage of a gene-independent heritability of behaviour is clear. It can mutate the behavioural phenotype at a much faster rate and to a more rigorous extent than genetic mechanisms in a changing environment. Once a particular information or behaviour is copied from a conspecific, it may still be modified and optimized by its positive or negative consequences for the single organism. By that way, particular behaviours can be completely erased from transmission, and new ones can be created and passed on. In constant or constructed “niches” (Laland et al. Reference Laland, Odling-Smee and Feldman2000), the advantage may be even bigger, because this way of passing knowledge to the next generation allows for an accumulation in the complexity of the behaviours (Byrne & Russon Reference Byrne and Russon1998). A multitude of complex human behaviours related to sophisticated technology, which essentially define cultural development, can only be passed on by copying (Boyd et al. Reference Boyd, Richerson and Henrich2011; Laland Reference Laland2004). The behavioural phenotype of an individual may thus be a function of the genome, “inherited behaviours,” environmental factors, and their specific interactions (Laland et al. 2010).