Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees

doi:10.1016/j.tig.2004.08.009

Trends in Genetics

Volume 20, Issue 11, November 2004, Pages 524-529

https://doi.org/10.1016/j.tig.2004.08.009 Get rights and content

The genomic DNA sequences of humans and chimpanzees differ by only 1.24%. Recently, however, substantial differences in gene-expression patterns between the two species have been revealed. In this article, we investigate the genomic distribution of such differences. Besides confirming previous findings about the evolution of sex chromosomes and duplications, we show that chromosomal rearrangements are associated with increased gene-expression differences in the brain and that rearrangements can have both direct and indirect effects on the expression of linked genes. In addition, our results are consistent with a role for some rearrangements in the original speciation events that separated the human and chimpanzee lineages.

Section snippets

Sex chromosomes and segmental duplications

An analysis pooling all tissues together showed that the levels of expression divergence differ significantly between chromosomes (Kruskal-Wallis, df=23, P<0.001; Figure 1). Two main factors that are known to influence sequence evolution and that, a priori, could also influence expression differences are the evolutionary dynamics of sex chromosomes relative to autosomes 8, 9 and segmental duplications 10, 11. Table 1 shows the average absolute FC in the expression level for all tissues

Chromosomal rearrangements

Since their separation from a common ancestor, six-to-seven million years ago, the genomes of humans and chimpanzees have diverged via chromosomal rearrangements, which are on a much larger scale than differences in nucleotide sequences or differences in gene expression. Although the extent of these differences awaits full-genome comparisons, ten major rearrangements can be detected in metaphase chromosomes [15]: they include nine pericentric inversions (human chromosomes 1, 4, 5, 9, 12, 15,

Direct versus indirect effects of rearrangements

Little is known about how alterations in expression patterns that are directly induced by rearrangements could extend along a chromosome and, thus, we cannot be sure that their positional effects have been properly assessed by the previous tests. Moreover, models of recombination-mediated effects of rearrangements 16, 24 also predict larger divergence around breakpoints, where gene-flow between different chromosomal arrangements has the strongest reduction. These questions can be evaluated by

Concluding remarks

The results presented here confirm that, when considering gene-expression divergence, sex-linked genes evolve under different pressures than autosomes and that duplicated genes tend to evolve faster than single-copy genes. Furthermore, we have shown that rearranged chromosomes have accumulated greater differences in brain gene-expression patterns between humans and chimpanzees than colinear chromosomes. Our results therefore suggest several conclusions. First, there is an association between

Acknowledgements

We thank A. Andrés, N. Barton, F. Calafell, J. Castresana, D. H. Geschwind, C. Lalueza and O. Lao for helpful discussions. We also thank C. Barlow and D. J. Lockhart for their contribution to the generation of the array data that was the basis of this study. We are indebted to L. Grossman, J. Hacia, M. Karaman, P. Khaitovich, S. Paabo and M. Uddin for making available the other array datasets used, and D. J. Lockhart for developing the BullFrog program. A.N. is supported by the Ramón y Cajal

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Citation Excerpt :
A subsequent study found that, for brain cortex tissue, gene expression divergence was higher within rearranged than within collinear chromosomes [67], a result confirmed by an independent study [68]. Just as in the case of sequence divergence, expression differences are largest around the inversion breakpoints [67]. Nonetheless, evidence based on sequence or gene expression divergence needs to be re-examined in the light of the recent simulations by Feder and Nosil [69], who studied the effects of CRs on gene flow after secondary contact.
The suggestion that chromosomal rearrangements play a role in speciation resulted from the observation that heterokaryotypes are often infertile. However, the first chromosomal speciation models were unsatisfactory and data available to test them was scarce. Recently, large amounts of data have become available and new theoretical models have been developed explaining how rearrangements facilitate speciation in the face of gene flow. Here, we re-examine theoretical predictions and revisit different sources of data. Although rearrangements are often associated with increased levels of divergence, unequivocal demonstration that their role in suppressing recombination results in speciation is often lacking. Finally, we question some previous predictions and suggest new empirical and theoretical approaches to understanding the relevance of rearrangements in the origin of species.
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Trends in Genetics

Genome AnalysisChromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees

Section snippets

Sex chromosomes and segmental duplications

Chromosomal rearrangements

Direct versus indirect effects of rearrangements

Concluding remarks

Acknowledgements

Trends Genet.

Trends Genet.

Trends Genet.

Am. J. Hum. Genet.

Am. J. Hum. Genet.

Cell

Evolution at two levels: molecular similarities and biological differences between humans and chimpanzees

Science

Intra- and interspecific variation in primate gene expression patterns

Science

Elevated gene expression levels distinguish human from non-human primate brains

Proc. Natl. Acad. Sci. U. S. A.

Regional patterns of gene expression in human and chimpanzee brains

Genome Res.

Comparative analysis of gene-expression patterns in human and african great ape cultured fibroblasts

Genome Res.

Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expresion profiles

Genetics

Sex biases in the mutation rate

Trends Genet.

Role of duplicate genes in genetic robustness against null mutations

Nature

Genome Analysis
Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees