Abstract
Author SummarySpecies evolution is often depicted as a slow and continuous process punctuated by rapid changes. One example of the latter is the evolution of human cognition–emergence of an exceedingly complex phenotype within a few million years. What genetic mechanisms might have driven this process? Nearly 40 years ago, it was proposed that human-specific gene expression changes, rather than changes in protein sequence, might underlie human cognitive evolution. Here we compare gene expression throughout postnatal brain development in humans, chimpanzees, and macaques. We find that simple changes in gene expression levels, plausibly driven by mutations in cis-regulatory elements, accumulate at similar rates in all three evolutionary lineages. What sharply distinguishes humans from other species is change in the timing and shape of developmental expression patterns. This is particularly pronounced in the prefrontal cortex, where 4-fold more genes show more human-specific developmental changes than chimpanzee-specific ones. Notably, our results indicate that this massive developmental remodeling of the human cortex, which affects hundreds of genes, might be driven by expression changes of only a few key regulators, such as microRNAs. Genes affected by this remodeling are preferentially associated with neural activity, thereby suggesting a link to the evolution of human cognition.
Highlights
In multicellular organisms, the evolution of novel characteristics frequently involves gene expression change [1]
Using a number of datasets, we found that two types of divergence, both expression differences that are constitutive throughout lifespan as well as expression differences involving changes in developmental patterns, have contrasting functional and evolutionary properties
In each brain region and species, we identified genes showing significant expression changes across the lifespan as well as genes showing significant expression divergence among species, using polynomial regression models and analysis of covariance, respectively (p,0.001, false discovery rate,10%)
Summary
The evolution of novel characteristics frequently involves gene expression change [1]. Several studies further associated these expression differences with neuron-specific functions [5,6,7], and a recent analysis of the human, chimpanzee, and macaque PFC transcriptomes reported more human-specific than chimpanzee-specific changes in developmental timing [8]. Together, these studies suggest that the human brain transcriptome has evolved at an accelerated rate compared to that of the chimpanzee, possibly reflecting the accelerated rate of human cognitive evolution. The molecular basis of human brain transcriptome acceleration, such as the contribution of cisand trans-events [9], remains unknown
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