BioProject

The X chromosome has a large effect on hybrid dysfunction, particularly hybrid male sterility. More...

The X chromosome has a large effect on hybrid dysfunction, particularly 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 loci than in their autosomal counterparts due to both natural selection and their hemizygosity in males (i.e. Faster-X effect), an effect that is expected to be greatest in genes with male-biased expression. Here I studied variation in transcript abundance within and between species in Drosophila yakuba, D. santomea and their hybrid males to evaluate both the faster-X and large-X effects at the level of genome-wide gene expression. I found that expression in X-linked male-biased genes evolves faster than in their autosomal counterparts, an effect that is accompanied by a unique reduction in gene expression polymorphism. Although we do not know the precise relationship between nucleotide and gene expression changes, elevated divergence to polymorphism ratios are consistent with Darwinian selection driving expression differences between species in X-linked male-biased genes, likely enhanced by male hemizygosity. Abundant changes in both cis- and trans-regulatory elements underlie regulatory gene expression divergence in the majority of the genes analyzed despite the recent split of the two sister species. I detected a large-X effect on regulation of expression in hybrid males, affecting mostly male-biased genes but also, to a lesser degree, nonsex-biased genes. Interestingly this misexpression is concentrated mostly in autosomal genes, likely facilitated by the rapid evolution of sex-linked trans-acting factors. I conclude that the faster evolution of X-linked male-biased genes, at both protein and expression levels, can contribute to explain the large effect of the X chromosome on hybrid male sterility, possibly mediating autosomal misexpression through cis-trans interactions. Overall design: 18 array study using total RNA (cDNA retranscribed with Oligo-dT) recovered from 1-day old adult males of three Drosophila yakuba and three D. santomea isofemale lines and the two reciprocal F1 hybrid males, with three-fold technical redundancy. Gene expression was estimated from a total of 12,442 protein-coding genes using 60-mer probes and an average of 10 probes per gene. Less...