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Faster‐X evolution of gene expression is driven by recessive adaptive cis‐regulatory variation in Drosophila

Llopart, Ana
Molecular ecology 2018 v.27 no.19 pp. 3811-3821
Drosophila yakuba, autosomes, evolutionary adaptation, gene dosage, gene expression, introns, loci, models, mutation, population genetics, prediction
The hemizygosity of the X (Z) chromosome fully exposes the fitness effects of mutations on that chromosome and has evolutionary consequences on the relative rates of evolution of X and autosomes. Specifically, several population genetics models predict increased rates of evolution in X‐linked loci relative to autosomal loci. This prediction of faster‐X evolution has been evaluated and confirmed for both protein coding sequences and gene expression. In the case of faster‐X evolution for gene expression divergence, it is often assumed that variation in 5′ noncoding sequences is associated with variation in transcript abundance between species but a formal, genomewide test of this hypothesis is still missing. Here, I use whole genome sequence data in Drosophila yakuba and D. santomea to evaluate this hypothesis and report positive correlations between sequence divergence at 5′ noncoding sequences and gene expression divergence. I also examine polymorphism and divergence in 9,279 noncoding sequences located at the 5′ end of annotated genes and detected multiple signals of positive selection. Notably, I used the traditional synonymous sites as neutral reference to test for adaptive evolution, but I also used bases 8–30 of introns <65 bp, which have been proposed to be a better neutral choice. X‐linked genes with high degree of male‐biased expression show the most extreme adaptive pattern at 5′ noncoding regions, in agreement with faster‐X evolution for gene expression divergence and a higher incidence of positively selected recessive mutations.