Evolution of genetic networks for human creativity

Abstract

The genetic basis for the emergence of creativity in modern humans remains a mystery despite sequencing the genomes of chimpanzees and Neanderthals, our closest hominid relatives. Data-driven methods allowed us to uncover networks of genes distinguishing the three major systems of modern human personality and adaptability: emotional reactivity, self-control, and self-awareness. Now we have identified which of these genes are present in chimpanzees and Neanderthals. We replicated our findings in separate analyses of three high-coverage genomes of Neanderthals. We found that Neanderthals had nearly the same genes for emotional reactivity as chimpanzees, and they were intermediate between modern humans and chimpanzees in their numbers of genes for both self-control and self-awareness. 95% of the 267 genes we found only in modern humans were not protein-coding, including many long-non-coding RNAs in the self-awareness network. These genes may have arisen by positive selection for the characteristics of human well-being and behavioral modernity, including creativity, prosocial behavior, and healthy longevity. The genes that cluster in association with those found only in modern humans are over-expressed in brain regions involved in human self-awareness and creativity, including late-myelinating and phylogenetically recent regions of neocortex for autobiographical memory in frontal, parietal, and temporal regions, as well as related components of cortico-thalamo-ponto-cerebellar-cortical and cortico-striato-cortical loops. We conclude that modern humans have more than 200 unique non-protein-coding genes regulating co-expression of many more protein-coding genes in coordinated networks that underlie their capacities for self-awareness, creativity, prosocial behavior, and healthy longevity, which are not found in chimpanzees or Neanderthals.

Fig. 1. Comparison of types of genes in 3 hominoid species.

Comparative analysis of the distinct types of genes (as defined in Supplementary Table S4) belonging to the Emotional reactivity, Self-control, and Self-awareness networks of genes present in (A) Chimpanzees (Pan troglodytes) (B) Neanderthals (Homo neanderthalensis) and (C) modern humans (Homo sapiens).

Fig. 2. Types of genes found only in modern humans.

Comparative analysis of the distinct types of genes (as defined in Supplementary Table S4) found exclusively in modern Homo sapiens: A Broad gene categories, B Fine-grained gene categories, and C Analysis of the genes from A in the genotypic networks associated with the Emotional-unreliable, Organized-reliable, and Creative-reliable phenotypic networks of modern humans.

Fig. 3. Brain regions in which genes found only in modern humans are overexpressed.

Normalized average gene expression in Allen Human Brain Atlas in particular regions of the human brain in which there is significant co-expression of the constituent genes of SNP sets in which there is at least one gene found only modern humans. The highlighted regions are called regions of interest (ROIs) because they are the regions in which a given list of genes are significantly co-expressed when compared to the rest of the Allen Human Brain Atlas. The color code indicates the importance of the region, with red as maximum. A and B depict ROIs in which constituent genes of the Character SNP sets of the self-awareness network are highly expressed, whereas C and D depict ROIs in which constituent genes of the Temperament SNP sets of the self-awareness network are highly expressed.