Evolution of Gene Expression in Human and Chimpanzee Brains

Abstract

It has long been proposed that for creating diverse phenotypes in closely related species, such as a striking difference between human and chimpanzee brain functions, evolutionary changes in gene expression are more important than the changes in protein structure. High‐throughput detection methods make it possible to gauge the differences in gene expression at the genome‐wide level. Initial studies using deoxyribonucleic acid microarrays have shown that gene expression evolution is more conserved in the brain than in other tissues. However, those studies have also shown that the divergence rate of gene expression in the brain is higher in humans than in the chimpanzee lineage. Subsequent studies have identified detailed differences in gene expression such as alterations in network connectivity and temporal order. In addition to the expression of protein‐coding genes, the expression of noncoding RNAs may also affect the divergence of gene expression and contribute to the phenotypic differences between humans and chimpanzees.

Key Concepts:

  • Differences in gene expression patterns rather than the changes in protein structures may have contributed to the functional differences between human and chimpanzee brains.

  • The set of genes that have different expression patterns in human and chimpanzee brains can be identified using high‐throughput methods such as DNA microarrays and RNA‐Seq.

  • Although we can detect functional gene expression changes specific to the human brain, it is not easy to elucidate the underlying evolutionary mechanisms.

  • Gene expression is a complex trait; understanding the molecular mechanisms of brain development is important to unveil the genetic basis of brain evolution.

  • Several studies revealed that the pattern of gene expression evolution in human brains was highly conservative in general, but showed acceleration after the split from the chimpanzee lineage.

Keywords: evolution; primates; DNA microarray; gene expression; brain; natural selection

Figure 1.

Phylogenetic tree of the primates of the group Catarrhini. The closest relatives of humans are chimpanzees (Pan troglodytes) and bonobos (Pan paniscus); however, some parts of the human genome are more closely related to the gorilla (Gorilla gorilla) genome.

Figure 2.

Divergence of gene expression between humans and chimpanzees in five tissues. Genes particularly expressed in the target tissues were analysed. The height of the bars represents the average expression divergence over all possible pairwise comparisons. Error bars show 95% confidence intervals estimated by bootstrap resampling. Reproduced from Khaitovich et al. .

Figure 3.

The number of genes expressed differentially between the lineages of the humans (open bars, H) and chimpanzees (solid bars, C) in the brain and the liver (P⩽.05). Orangutans were used as the outgroup. The data were obtained by Enard et al. and reanalysed by Gu and Gu .

Figure 4.

Human‐specific hub genes identified by module visualisation. (a) Three hundred pairs of genes with the greatest connectivity in the human cortex are represented by thin lines. Genes with negatively correlated expression levels are connected by thick lines. (b) Connections from (a) that are specific to the human cortex. Reproduced from Oldham et al. with permission from the National Academy of Sciences, USA.

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Vallender EJ, Mekel‐Bobrov N and Lahn BT (2008) Genetic basis of human brain evolution. Trends in Neurosciences 31: 637–644.

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Osada, Naoki, Sumio, Sugano, and Suzuki, Yutaka(Apr 2013) Evolution of Gene Expression in Human and Chimpanzee Brains. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020748.pub2]