Abstract
Microarray technologies allow the identification of large numbers of expression differences within and between species. Although environmental and physiological stimuli are clearly responsible for changes in the expression levels of many genes, it is not known whether the majority of changes of gene expression fixed during evolution between species and between various tissues within a species are caused by Darwinian selection or by stochastic processes. We find the following: (1) expression differences between species accumulate approximately linearly with time; (2) gene expression variation among individuals within a species correlates positively with expression divergence between species; (3) rates of expression divergence between species do not differ significantly between intact genes and expressed pseudogenes; (4) expression differences between brain regions within a species have accumulated approximately linearly with time since these regions emerged during evolution. These results suggest that the majority of expression differences observed between species are selectively neutral or nearly neutral and likely to be of little or no functional significance. Therefore, the identification of gene expression differences between species fixed by selection should be based on null hypotheses assuming functional neutrality. Furthermore, it may be possible to apply a molecular clock based on expression differences to infer the evolutionary history of tissues.
MeSH Terms
Animals
Biological Evolution
Brain/metabolism
DNA, Complementary/metabolism
Evolution, Molecular
Gene Expression Regulation
Liver/metabolism
Models, Biological
Models, Genetic
Oligonucleotide Array Sequence Analysis
Pan troglodytes
Phenotype
Pseudogenes
RNA, Messenger/metabolism
Species Specificity
Stochastic Processes
Time Factors
Tissue Distribution
Chemicals
DNA, Complementary
RNA, Messenger
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Khaitovich Philipp
Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany.
Weiss Gunter
Lachmann Michael
Hellmann Ines
Enard Wolfgang
Muetzel Bjoern
Wirkner Ute
Ansorge Wilhelm
Pääbo Svante
Conflict of Interest
The authors have declared that no conflicts of interest exist.
References (26)
26 references, click to expand
-
Functional discovery via a compendium of expression profiles.
Cell. 2000 Jul 7;102(1):109-26
PMID: 10929718
-
Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees.
Am J Hum Genet. 2001 Feb;68(2):444-56
PMID: 11170892
-
Delineating developmental and metabolic pathways in vivo by expression profiling using the RIKEN set of 18,816 full-length enriched mouse cDNA arrays.
Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2199-204
PMID: 11226216
-
Initial sequencing and analysis of the human genome.
Nature. 2001 Feb 15;409(6822):860-921
PMID: 11237011
-
Large-scale analysis of the human and mouse transcriptomes.
Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4465-70
PMID: 11904358
-
BLAT--the BLAST-like alignment tool.
Genome Res. 2002 Apr;12(4):656-64
PMID: 11932250
-
Intra- and interspecific variation in primate gene expression patterns.
Science. 2002 Apr 12;296(5566):340-3
PMID: 11951044
-
Variation in gene expression within and among natural populations.
Nat Genet. 2002 Oct;32(2):261-6
PMID: 12219088
-
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
Bioinformatics. 2003 Jan 22;19(2):185-93
PMID: 12538238
-
Induced gene expression in human brain after the split from chimpanzee.
Trends Genet. 2003 Feb;19(2):63-5
PMID: 12547510
-
Evolution of gene expression in the Drosophila melanogaster subgroup.
Nat Genet. 2003 Feb;33(2):138-44
PMID: 12548287
-
TM4: a free, open-source system for microarray data management and analysis.
Biotechniques. 2003 Feb;34(2):374-8
PMID: 12613259
-
Estimation of divergence times for major lineages of primate species.
Mol Biol Evol. 2003 Mar;20(3):424-34
PMID: 12644563
-
A neutral explanation for the correlation of diversity with recombination rates in humans.
Am J Hum Genet. 2003 Jun;72(6):1527-35
PMID: 12740762
-
Sex-dependent gene expression and evolution of the Drosophila transcriptome.
Science. 2003 Jun 13;300(5626):1742-5
PMID: 12805547
-
Elevated gene expression levels distinguish human from non-human primate brains.
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13030-5
PMID: 14557539
-
Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expression profiles.
Genetics. 2003 Oct;165(2):747-57
PMID: 14573485
-
Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome.
Genome Res. 2003 Dec;13(12):2541-58
PMID: 14656962
-
A genome-wide survey of human pseudogenes.
Genome Res. 2003 Dec;13(12):2559-67
PMID: 14656963
-
Microarray analysis supports a role for ccaat/enhancer-binding protein-beta in brain injury.
J Biol Chem. 2004 Apr 2;279(14):14409-17
PMID: 14736879
-
PHENOTYPIC EVOLUTION BY NEUTRAL MUTATION.
Evolution. 1986 Sep;40(5):915-935
PMID: 28556213
-
NATURAL SELECTION AND RANDOM GENETIC DRIFT IN PHENOTYPIC EVOLUTION.
Evolution. 1976 Jun;30(2):314-334
PMID: 28563044
-
RATE TESTS FOR SELECTION ON QUANTITATIVE CHARACTERS DURING MACROEVOLUTION AND MICROEVOLUTION.
Evolution. 1988 Sep;42(5):1085-1089
PMID: 28581161
-
The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.
Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):581-98
PMID: 42062
-
Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA.
Mol Biol Evol. 1996 Sep;13(7):1044-53
PMID: 8752012
-
Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
Mol Biol Cell. 1998 Dec;9(12):3273-97
PMID: 9843569