Genomic imprinting and the social brain

Abstract

Genomic imprinting refers to the parent-of-origin-specific epigenetic marking of a number of genes. This epigenetic mark leads to a bias in expression between maternally and paternally inherited imprinted genes, that in some cases results in monoallelic expression from one parental allele. Genomic imprinting is often thought to have evolved as a consequence of the intragenomic conflict between the parental alleles that occurs whenever there is an asymmetry of relatedness. The two main examples of asymmetry of relatedness are when there is partiality of parental investment in offspring (as is the case for placental mammals, where there is also the possibility of extended postnatal care by one parent), and in social groups where there is a sex-biased dispersal. From this evolutionary starting point, it is predicted that, at the behavioural level, imprinted genes will influence what can broadly be termed bonding and social behaviour. We examine the animal and human literature for examples of imprinted genes mediating these behaviours, and divide them into two general classes. Firstly, mother-offspring interactions (suckling, attachment and maternal behaviours) that are predicted to occur when partiality in parental investment in early postnatal offspring occurs; and secondly, adult social interactions, when there is an asymmetry of relatedness in social groups. Finally, we return to the evolutionary theory and examine whether there is a pattern of behavioural functions mediated by imprinted genes emerging from the limited data, and also whether any tangible predictions can be made with regards to the direction of action of genes of maternal or paternal origin.

Figure 1

A diagram showing how asymmetries of relatedness can occur through multiple paternity of a female's offspring, and in a simple matrilineal society with sex-biased dispersal. (a) With multiple paternity either within a brood or, as is more likely, across a female's reproductive lifetime, offspring from the same mother differ in their relatedness owing to the presence of different paternal genomes. (b) Schematic of a simple matrilineal society as described in the text. Males, coming in from outside the group, hold short breeding tenure (matings with females are indicated by thin arrows). Male offspring (not shown) leave the group when sexually mature. What can be seen is that all females share, to differing degrees, maternally derived genes (in red)—this would of course also be true for male offspring. However, paternally derived genes are only present in the strata of the social group and are not shared as widely.