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Mol Biol Evol. 2015 Oct;32(10):2605-15. doi: 10.1093/molbev/msv135. Epub 2015 Jun 2.

Molecular Mechanisms and Evolutionary Processes Contributing to Accelerated Divergence of Gene Expression on the Drosophila X Chromosome.

Author information

1
Department of Ecology and Evolutionary Biology, University of Michigan jcoolon@wesleyan.edu wittkopp@umich.edu.
2
Department of Computational Medicine and Bioinformatics, University of Michigan.
3
Department of Biological Sciences, Carnegie Mellon University Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center.
4
Department of Molecular, Cellular, and Developmental Biology, University of Michigan.
5
Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center.
6
Department of Ecology and Evolutionary Biology, University of Michigan Department of Computational Medicine and Bioinformatics, University of Michigan Department of Molecular, Cellular, and Developmental Biology, University of Michigan jcoolon@wesleyan.edu wittkopp@umich.edu.

Abstract

In species with a heterogametic sex, population genetics theory predicts that DNA sequences on the X chromosome can evolve faster than comparable sequences on autosomes. Both neutral and nonneutral evolutionary processes can generate this pattern. Complex traits like gene expression are not predicted to have accelerated evolution by these theories, yet a "faster-X" pattern of gene expression divergence has recently been reported for both Drosophila and mammals. Here, we test the hypothesis that accelerated adaptive evolution of cis-regulatory sequences on the X chromosome is responsible for this pattern by comparing the relative contributions of cis- and trans-regulatory changes to patterns of faster-X expression divergence observed between strains and species of Drosophila with a range of divergence times. We find support for this hypothesis, especially among male-biased genes, when comparing different species. However, we also find evidence that trans-regulatory differences contribute to a faster-X pattern of expression divergence both within and between species. This contribution is surprising because trans-acting regulators of X-linked genes are generally assumed to be randomly distributed throughout the genome. We found, however, that X-linked transcription factors appear to preferentially regulate expression of X-linked genes, providing a potential mechanistic explanation for this result. The contribution of trans-regulatory variation to faster-X expression divergence was larger within than between species, suggesting that it is more likely to result from neutral processes than positive selection. These data show how accelerated evolution of both coding and noncoding sequences on the X chromosome can lead to accelerated expression divergence on the X chromosome relative to autosomes.

KEYWORDS:

cis-regulation; faster-X; gene expression; selection; trans-regulation

PMID:
26041937
PMCID:
PMC4592344
DOI:
10.1093/molbev/msv135
[Indexed for MEDLINE]
Free PMC Article

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