Journal article
The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids
Molecular biology and evolution, Vol.29(12), pp.3873-3886
12/2012
DOI: 10.1093/molbev/mss190
PMID: 22844069
Abstract
The X chromosome has a large effect on hybrid dysfunction, particularly on hybrid male sterility. Although the evidence for this so-called large-X effect is clear, its molecular causes are not yet fully understood. One possibility is that, under certain conditions, evolution proceeds faster in X-linked than in autosomal loci (i.e., faster-X effect) due to both natural selection and their hemizygosity in males, an effect that is expected to be greatest in genes with male-biased expression. Here, I study genome-wide variation in transcript abundance between Drosophila yakuba and D. santomea, within these species and in their hybrid males to evaluate both the faster-X and large-X effects at the level of expression. I find that in X-linked male-biased genes (MBGs) expression evolves faster than in their autosomal counterparts, an effect that is accompanied by a unique reduction in expression polymorphism. This suggests that Darwinian selection is driving expression differences between species, likely enhanced by the hemizygosity of the X chromosome in males. Despite the recent split of the two sister species under study, abundant changes in both cis- and trans-regulatory elements underlie expression divergence in the majority of the genes analyzed, with significant differences in allelic ratios of transcript abundance between the two reciprocal F(1) hybrid males. Cis-trans coevolution at molecular level, evolved shortly after populations become isolated, may therefore contribute to explain the breakdown of the regulation of gene expression in hybrid males. Additionally, the X chromosome plays a large role in this hybrid male misexpression, which affects not only MBG but also, to a lesser degree, nonsex-biased genes. Interestingly, hybrid male misexpression is concentrated mostly in autosomal genes, likely facilitated by the rapid evolution of sex-linked trans-acting factors. I suggest that the faster evolution of X-linked MBGs, at both protein and expression levels, contributes to explain the large effect of the X chromosome on hybrid male sterility, likely mediating widespread autosomal misexpression through the preferential recognition of cis-regulatory elements by conspecific trans-acting factors (i.e., cis-trans conspecific recognition).
Details
- Title: Subtitle
- The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids
- Creators
- Ana Llopart - Department of Biology, University of Iowa, USA. ana-llopart@uiowa.edu
- Resource Type
- Journal article
- Publication Details
- Molecular biology and evolution, Vol.29(12), pp.3873-3886
- Publisher
- United States
- DOI
- 10.1093/molbev/mss190
- PMID
- 22844069
- ISSN
- 1537-1719
- eISSN
- 1537-1719
- Language
- English
- Date published
- 12/2012
- Academic Unit
- Biology
- Record Identifier
- 9983992064602771
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