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Evolution of primate gene expression

Key Points

  • Gene expression patterns differ substantially among even closely related primate species.

  • The extent of transcriptome divergence between species increases monotonically with evolutionary time since their divergence.

  • The extent of divergence of overall gene expression between species differs among tissues and, in a given tissue, parallels the extent of divergence of the amino-acid sequences of proteins expressed in that tissue.

  • A neutral theory of evolution, where divergence is primarily determined by negative selection and time since divergence, seems to be an adequate and useful null hypothesis for evolutionary analyses of the transcriptome.

  • Genes expressed in the testes have experienced positive selection both with respect to their expression and to their sequences among primates.

  • Gene expression in the brain has diverged less than that of other tissues analysed to date, but a tendency for acceleration of changes on the human lineage relative to the chimpanzee lineage could indicate positive selection.

Abstract

It has been suggested that evolutionary changes in gene expression account for most phenotypic differences between species, in particular between humans and apes. What general rules can be described governing expression evolution? We find that a neutral model where negative selection and divergence time are the major factors is a useful null hypothesis for both transcriptome and genome evolution. Two tissues that stand out with regard to gene expression are the testes, where positive selection has exerted a substantial influence in both humans and chimpanzees, and the brain, where gene expression has changed less than in other organs but acceleration might have occurred in human ancestors.

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Figure 1: Expression divergence between humans and chimpanzees in different tissues.
Figure 2: Negative selection adds up across tissues.
Figure 3: Hierarchical clustering of expression differences between humans and chimpanzees in five different tissues.

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Acknowledgements

The authors thank R.E. Green and S.E. Ptak for many helpful comments on the manuscript and all members of our group for fruitful discussions. The research on primate gene expression in our laboratory is supported by the Max Planck Society and the Bundesministerium für Bildung und Forschung.

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FURTHER INFORMATION

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Glossary

Negative selection

Removal of genetic variants in a population that decrease the fitness of their carrier. If negative selection acts on a phenotypic trait, this is also called stabilizing selection.

Positive selection

Increase in frequency of a genetic variant or a phenotypic trait because it increases the fitness of its carrier. If positive selection acts on a phenotypic trait, this is also called directional selection.

Sperm competition

The direct competition between sperm from different males that occurs when females copulate with multiple males.

Meiotic drive

Preferential transmission of one of two alleles from a parent to its offspring.

Outgroups

Species that are more distantly related to two or more species studied and can therefore be used to estimate the ancestral state of a trait such as nucleotide sequence or gene expression level.

Linkage disequilibrium

Non-random association of nucleotide polymorphisms along the chromosome. Larger areas of stronger linkage disequilibrium are seen around a genetic change that has been positively selected in the recent past.

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Khaitovich, P., Enard, W., Lachmann, M. et al. Evolution of primate gene expression. Nat Rev Genet 7, 693–702 (2006). https://doi.org/10.1038/nrg1940

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